Nematoda : Heteroderidae) and the Roots of a Tropical Rainforest Tree
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An unique host-parasite relationship between HyZonema ivorense .(Nematoda : Heteroderidae) and the roots of a tropical rainforest tree Donald P. TAYLOR,Patrice CADET and Michel Luc Laboratoire de Nématologie, ORSTOM, B. P. 1386, Dakar, Sénégal; Laboratoire de Nématologie, ORSTOM, B. P. V 51, Abidjan, Côte d’Ivoire; Muséum national d’Histoire naturelle, Laboratoire des Vers, 43 rue Cuvier, 75 008 Paris. SUMMARY Roots of young avodire (Turraeanfhus africana), a member of the Meliaceae used as a source of lumber, were observed in Ivory Coast to have slight swellings frequently with a small necrotic depression. Dissection of thesc swellings revealed the presence of a.necrotic tunnel leading from the necrotic depression to a saccate female of Hylonema ivorense usually located near the vascular system. Histological examination of infected roots showed that each female incited production of only one giant cell, each giant ce11 m‘as uninucleate, each nucleus was greatly enlarged-up to 200 times the volume of a normal nucleus, and each nucleus contained an enlarged nucleolus itself usually larger than a healthy nucleus. No discrete ce11 wall was observed surrounding the giant cell. Xylem tissue near infection sites was abnormal. Eggs, and occasionally juveniles, were lound throughout the tunnel. Although a suitable host-parasite relation exists, infected tissueis characterized by considerable necrosis. Giant ce11 formation and nuclear enlargement were detected in ten-day-old material. Enlargementof these structures continued through 40 days. Two additionalhosts, Neuropeltisprevosteoides and Khayaivorensis, exhibitedthe same symptoms. Tabernaemontana crassa was also observed to be naturally infected. RÉSUMÉ Un mode unique de relations parasitaires chez Ilylonema ivorense (Nematoda : Heteroderidae) attaquan.t les racines d’un arbre de la forêt tropicale humide. ’ Les racines de jeunes avodirés (Turraeanthus africana, Meliacées), essence exploitée en Côte d’Ivoire pour l’ébénis- terie, montraient de légers renflements souvent accompagnés en surface d’une dépression nécrotique.A la dissection, ces renflements ont révélé la présence d’un tunnel nécrotique conduisant de la dépression à une femelle renflée de Hylonema ivorense, généralement localisée près du cylindre central. L’étude histologique des racines infestées a montré que chaquefemelle induit la formation d’une cellule géante unique, possédant un seul noyau anormalement développé (plus de 200 fois le volume d’un noyau normal) contenant lui-même un nucléole hypertrophié, d’une taille supérieure à celle d’un noyau normal. Aucune paroi, même discrète, n’a été observée autour des cellules géantes. Les tissus du xylème sont perturbés autour des sites d’infestation. Des ceufs et occasionnellement des juvénilesont été observés à l’intérieurdu tunnel. Bien qu’un modederelation hôte/parasite efficace paraisse exister, les tissus infestés sont caractérisés par l’étendue considérable des zones nécrotiques. La formation des cellules géantes et l’hypertrophie de leur noyau ont pu observéesêtre sur du matériel végétal n’ayantpas plus de dix jours, ces phénomènes se poursuivant pendant 40 jours. Deux autres plantes hôtes, Neuropeltis prevosteoides et Khayaivorensis, présententles mêmes symptômes. Tabernaenzontanacrassa estégalement infesté en milieu naturel. Cellular responses of plants to plant-parasitic effectsof parasitismvary greatly depending nematodeshave been thoroughly reviewed upon the species of nematodeinvolved. [Dropkin, 1969), from which it is obvious that Members of theHeteroderidae (Filipjev & SchuurmansStekhoven, 1941) Skarbilovich, 1947 andthe Meloidogynidae(Skarbilovich, (l) A portion of thispaper was presented at the XIIIthInternational Nematology Symposium, 1959) Wouts,1973 induce the most profound Dublin,Ireland, 5-11 September 1976. anatomical changeshost. thein Members of Rev. Nématol. 1 (1) : 99 à 108 (1978) 99 D. P. Taylor, P. Cadet & M. Luc the genus Meloidogyne Goeldi,1892 usually swellingswere cutand fixed inFAA for72 produce root galls characterized by hypertrophy hours or longer. They were then embedded in and hyperplasia of various tissues and by the paraffin, sectioned at 15 or 18 pm and stained presence of large, multinucleate giant cells, or with safranin and fast green. Photographs were syncytia (Dropkin, 1969). Members of the genus taken with a Leitz “Orthomat” photomicroscope. Heferodera Schmidt, 1871 normally do not Additional fixedroots were dissected by hand induce galls, but the histopathology of infection to further study the relationship. sitesis similar tothat of hleloidogyne. It is To studysymptom development, seeds of generally conceded that these syncytia, two to T. africana weregerminated and seedlings many perinfection, are formed by fusion of transplantedtosterile soil. Suspensions of cells at thefeeding site resulting in the formation H. ivorense juveniles were poured over the soil of abnormallyenlarged, multinucleate cells surfacearound the seedlings.One infected (Rohde & McClure, 1975). Mitoticdivision, plant wassacrificed every five daysand the frequentlyreported to be synchronous, con- infected roots were fixed, sectioned and stained tributesto the multinucleate condition ; in as described above. certain 1Weloidogyne infectionssyncytia have been reported tohave “hundreds of nuclei” (Dropkin,1969). These nuclei arefrequently enlarged, sometimes one hundred times normal Results (Krusberg & Nielsen, 1958 ; Dropkin & Nelson, 1960).Nucleoli are also frequently enlarged in OBSERVATIONS ON NATURALLY INFECTED Meloidogyne infections and have been reported ROOTS to beas large asnormal nuclei (Krusberg & Nielsen,1958). Thehost-parasite relations of Nucleus and nucleolus. Figure 1 illustratesa iVIeloidodera floridensis has been partially de- giant ce11 inducedby H. ivorense in a root of scribed byRuehle (1962), Who statedthat T. africana. The mostconspicuous feature of this “giant cells adjacent to the female nematode” ce11 is the enlargement of the single nucleus (N), are produced but no mention was made of their especiallywhen compared to the size of the nuclear condition. The histopathology induced nucleus (n)in an adjacent unaffected cell. by othermembers of the Heteroderidae,i.e. When 25 nucleifrom similar giant cells were CryphoderaColbran, 1966, Afalodera Wouts & measuredtheir mean diameters were 78 x Sher, 1971, Sarisodera Wouts & Sher, 1971 and 59 pm ; normal nucleimeasured 11 x 10 Pm. Hylonema Luc, Taylor & Cadet, 1978, has not Caicuiation of the voiume of the iarger nuclei been described. indicate that the mass of thesenuclei can be Thehistopathology of roots of thetropical more than 200 times that of normalnudei. rainforest tree, avodiré, infected withHylonema Thesingle, deeply staining nucleolus (NU) is ivorense Luc,Taylor & Cadet,1978, is unlike also greatly enlarged, 17 x 15.5 pm, compared any known caused by a member of t8he Hetero- to a diameter of less than 1.6 in healthy cells. deridae and is, therefore, described in detail. In examining hundreds of giant cells, no case of multiple nuclei was observed. Giant cells. Examples of H. ivorense-induced Materials and Methods giant cells are shown in Figures 1-4. Giant cells werefound in the cortex (Fig. 1), adjacent to Soi1 and root sampleswere collected from the vascular tissue(= pericycle?) as in Figure3, avodiré,Turraeanthus africana Pellegr. , a and within the vascular tissue (Figure 4 illus- member of the Meliaceae, growing in a tropical trates a giant ce11 surrounded by xylem tissue). rainforestreserve at Banconear Abidjan, These cells areirregular in outline, although IvoryCoast. Nematodes were extractedby inthe xylem they are generallyelongated in standardtechniques. Small swellings,each the direction of the root axis (Fig. 4). They are usually with a small necrotic depression, were extremely variable in size and lengths of over notedon the roots.Root pieces exhibiting 350 pm have beenmeasured. Inaddition to 1O0 Rev. Nématol. 1 (1) : 99 ci 108 (1978) Host-parasite relationships in Hylonema ivorense Fig. 1-4 : Giant cells induced by Hylonema ivorense in roots of Turraeanthus africana (g = giant ce11 ; N = enlarged nucleus ; NU = enlarged nucleolus ; n = normal nucleus ; nu = normal nucleolus). Fig. 5-6 : Xylem tissue in roots of T. africana; 5 : non-infected root portion; 6 : root infected with H. ivorense. Rev. Némaiol. 1 (1) : 99 à 108 (1978) 1O1 D. P. Taylor, P. Cadet & M. Luc being uninucleate, as previously mentioned, the intothe giant ce11 nearthe enlargednucleus giant ce11 ischaracterized bydense, deeply (Fig. 3). Acast juvenile cuticle can often be stainingcytoplasm. No discrete ce11Wall has seen surroundingthe lip region (Fig. 11, 12, been observed surrounding giant cells (Fig. 1-3). 13 and 15). Inmany casesobserved there The apparent “wall” in Figure 4 was, in fact, appears to be another structure surrounding the composed of the ce11 walls of adjacentxylem anterior end of the nematode which, based upon tissue. It must be emphasized that in no case stainingreaction, is presumed to be of plant was more than one giant ce11 associated with a origin(Fig. 10and 11). In Figure 12, the an- single nematode. When more than one giant ce11 terior end of thenematode (1) isobviously was observed in a root section, examination of withinan annulated juvenile cuticle (2) with adjacent serial sectionsalways demonstrated the a distinct lipregion ; however, theother presence of multiple infections.Cortical cells structure (3) has no distinct morphology to adjacent.to or nearthe giant cells