Trends in Biosciences 10(25), Print : ISSN 0974-8431, 5285-5290, 2017

Host Diversity and Affinity in Xiphinema americanum Y.S. RATHORE

Indian Institute of Pulses Research, Kanpur, Uttar Pradesh email : [email protected]

ABSTRACT ectoparasite and all the life stages feed at the root tips of Xiphinema americanum (Nematoda: Longidoridae) is a plants and attached to young growing roots due to source- sink dynamics (Wikipedia, 2017a). While penetrating into migratory ectoparasite and widely distributed all over the world. Besides causing direct damage, it also transmits plant cells, nematode secretes enzymes that results in cell plant viruses and cause economic losses to crops and hypertrophy and thickening, and then it is able to extract orchard plants. Its host range includes 200 angiosperms cell cytoplasm (Norton and Hoffman 1974). Plants exhibit and 22 gymnosperms species. Results on host diversity poor growth and/or stunting, yellowing or wilting of foliage, and affinity in traditional taxonomic system of Hutcinson reduced root systems, lack of secondary roots and (1973) and recent system APG IV (2016) revealed greater occasional tufts of secondary roots (Christie, 1959, Cohn, preference to fundamentally woody plants. In Hutchinson’s 1970). Moderately swelling of roots with clusters of shoots, stubby branches was observed in pine trees (Cohn, 1970, system nematode selected 72.52% plants from , 17.51% and 9.91% White, 1955) and complete defoliation in coffee trees gymnosperms. Among dicotyledons, plants from lignosae (Lordello, 1972).This nematode has also implicated in (fundamentally woody plants) showed greater preference transmitting viral diseases to several crops.It is a C-rated (58.11%) than herbaceae (fundamentally herbaceous pest in California due to its wide host range of California plants (14.41%). Glumiflores in were preferred crops. Jones et al (2013) described as eighth economically more than others in the group. However, in APG IV system important to agricultural crops in the World. maximum (41.44%) plants were parasitized in Rosids, Ferris (2011)reported that X. americanum is a non- followed by Asterids (21.62%), Monocots (17.59%) and specific plant nematode and have over one hundred then followed by gymnosperms (9.91%). Specific different plant hosts. However, in earlier studies of host Affiliation Index and species: family ratio manifested preference of other nematode species viz., Meloidogyne greater affinity to plants in (/ inconita (Rathore and Ali, 2014), Helicotylenchus spp. Leguminales), Rosaceae (), Poaceae (Monocots) (Rathore and Tiwari, 2015) Heterodera spp. (Rathore and and Pinaceae (gymnosperms). It appears that X. Tiwari, 2015a), Paratylenchus spp. (Rathore and Tiwari, americanum co-evolved with these four families in 2015b), different species of Root-knot nematodes (Rathore different ecological niches or geographical areas. and Tiwari, 2016), and Aphelenchoides spp. (Rathore and Tiwari, 2016a) have showed their affinity to certain Key Words APG IV system, Lignosae, Herbaceae, taxonomic groups of host plants and even in some cases Dicotyledons, Monocotyledons, indicated evolutionary lineage of host groups. In the Angiosperms, Gymnosperms, Dagger present study author has tried to examine the host range nematode pattern of this nematode and its affinity to any particular taxonomic group (s). Xiphinema americanum (Nematoda: Enola: MATERIALS AND METHODS Longidoridae), commonly known as Xiphinema, Dagger Host plants of X. americanum were downloaded from nematode, American Dagger nematode, is a plant internet (Nemaplex, 2017). All the plant species were aligned pathogenic nematode. However, X.americanum is to different families and orders as described by Hutchinson comprised several species which are difficult to distinguish (1973) and APG IV system of 2016 (Wikipedia, 2017). morphologically and biochemically. Therefore, this group Hutchinson in his classification divided angiosperms into of species is known as X. americanum sensu loto (s.l.) and two subphyla- dicotyledons and monocotyledons. the one which was first described by Cobb 1913 as X. Dicotyledons were partitioned into lignosae (fundmentally americanum sensu sricto (s.s.) Cobb 1913 (IPPC 2016). woody plants) and herbaceae (fundamentally haerbaceous Following description, therefore, pertains to X. americanum plants). Similarly, monocotyledons were divided into (s.l.). This nematode is widely distributed and found in all calyciferae (with a distinct calyx and corolla), corolliferae the continents except Antarctica. The region of highest (calyx and corolla are more or less similar), and glumiflorae population is Eastern United States (Robbinson, 1993). (perianth is much more reduced or represented by lodicules). Other countries include Australia, Belize, Chile, Guatemala, Host species other than angiosperms were grouped as India, Japan, Korea, Mexico, New Zealand, Pakistan, South gymnosperms. To compare the host diversity in newer Africa, Sri Lanka, Uruguay and areas of Caribbean (Tarjan, system of classification of flowering plants i.e. Angiosperms 1969) but found frequently in Australiana and Oceania phylogeny Group (APG) IV described in 2016 was employed. (Hockland and Prior, 2009,CABI, 2013). It is a migratory Host affinity to any taxonomic group was judged by 5286 Trends in Biosciences 10 (25), 2017

Table 1. Distribution of host species in different taxonomic groups in Hutchinson’s system

Taxonomic groups Host species Genera Families Orders SAI Dicot-Lignosae 129 (58.11) 86 (53.75) 42 (57.53) 30 (55.56) 0.829 Dicot-Herbaceae 32 (14.41) 29 (18.13) 15 (20.55) 12 (22.22) 0.607 Monocot-Calyciferae 4 ( 1.80) 4 ( 2.50) 4 ( 5.48) 1 ( 1.85) 0.667 Monocot-Corolliferae 12 ( 5.41) 10 ( 6.24) 6 ( 8.22) 6 (11.11) 0.636 Monocot-Glumiflorae 23 (10.36) 18 (11.25) 1 ( 1.37) 1 ( 1.85) 1.25 Gymnosperms 22 ( 9.91) 13 ( 8.13 5 ( 6.85) 4 ( 7.41) 1.091 Figures in parantheses are % values

Table 2. Affiliation of host species to different taxonomic groups in Hutchinson’s system

Host order Taxonomic groups No. Host spp. (1) Dicot-L: Magnoliaceae (1) Magnolia sp. 1 Dicot-L: Lauraceae (3) Persea americana, Persea sp., (3) Umbellularia californica 3 Rosales (6) Dicot-L: Rosaceae (25) 25 Leguminales (7) Dicot-L: Caesalpiniaceae (2), Fabaceae (15) 17 Dicot-L: (1) Escallonia sp., Hydrangeaceae (1), Cunoniales (8) Hydrangea sp. 2 Araliales (10) Dicot-L: (3), Caprifoliaceae (1) 4 (11) Dicot-L: Buxaceae (1), (1), Piatanaceae (1) 3 Salicales (12) Dicot-L: (3) Populus lombardi, Populus sp., Salix sp. 3 (16) Dicot-L: Corylaceae (1), Fagaceae (4) 5 Juglandales (17) Dicot-L: Juglandaceae (3) 3 (19) Dicot-L: Moraceae (5), Ulmaceae (3) 8 Thymelaeles (21) Dicot-L: Nyctaginaceae (1) Bougainvillia sp. 1 (22) Dicot-L: (1) Macadamia sp. 1 Passiflorales (29) Dicot-L: (1)Passiflora sp. 1 Cucrbitales (30) Dicot-L: Begoniaceae (1), Cucurbitaceae (2) 3 Cactales (31) Dicot-L: Cactaceae (1) 1 Tiliales (32) Dicot-L: (1) 1 (33) Dicot-L: Malvaceae (2) 2 Euphorbiales (35) Dicot-L: Euphorbiaceae (1) 1 (36) Dicot-L: Theaceae (2) Camellia japonica, Camellia sp. 2 (38) Dicot-L: (7) 7 (40) Dicot-L: Myrtaceae (3), Punicaceae (1) 4 (41) Dicot-L: Aquifoliaceae (1) Ilex sp. 1 (44) Dicot-L: Elaeagnaceae (1), Rhamnaceae (1), (7) 9 Ebenales (46) Dicot-L: Ebenaceae (1) 1 Rutales (47) Dicot-L: (6) 6 (49) Dicot-L: Anacardiaceae (3), Sapindaceae (2) 5 Loganiales (50) Dicot-L: (6) 6 Apocynales (51) Dicot-L: Apocynaceae (2) 2 Rubiales (52) Dicot-L: (1) Gardenia sp. 1 (55) Dicot-H: Paeoniaceae (1) Paeonia sp. 1 (60) Dicot-H: (2) 2 (62) Dicot-H: Aiozaceae (1) Mesembryanthemum sp. 1 Chenopodiales (64) Dicot-H: (1), Chenopodiaceae (1) 2

RATHORE, Host Diversity and Affinity in Xiphinema americanum 5287

Host order Taxonomic groups No. Host spp. Onagrales (65) Dicot-H: Onagraceae (1) Fuschsia sp. 1 Dicot-H: (1) Crassula sp., (1) (69) sp. 2 Umbellales (72) Dicot-H: (1) Daucus carota 1 Valerianales (73) Dicot-H: Dipsacaceae (1)Dipsacus sp. 1 (76) Dicot-H: (12) 12 (77) Dicot-H: Convolvulaceae (1), (4) 5 (79) Dicot-H: Geraniaceae (1) Pelargonium sp. 1 (82) Dicot-H: Lamiaceae (3) 3 Monocot-Caly: Cannaceae (1), (1), (1), (94) (1) 4 (95) Monocot-Cor: (1) Lilium sp. 1 (97) Monocot-Cor: (4) 4 Amaryllidales (99) Monocot-Cor: (2) 2 Iridales (100) Monocot-Cor: Iridaceae (2) 2 Agavales (102) Monocot-Cor: Agavaceae (2) 2 Palmales (103) Monocot-Cor: (1) 1 Graminales (111) Monocot-Glu: Poaceae (23) 23 Cupressales Gym: Taxaceae (1)Taxus sp. 1 Equisetales Gym: Equisetaceae (1) Equisetum sp. 1 Pinales Gym: Cupressaceae (8), Pinaceae (11) 19 Polypodiales Gym: Polypodiaceae (1) Polypodiaceae sp. 1

Dicot-L=Dicotyledons-lignosae, Dicot-H=Dicotyledons-herbaceae, Monocot-Caly=Monocotyledons- calyciferae, Monocot- Cor=Monocotyledons-corolliferae, Monocot-Glu=Monocotyledons- glumiflorae, Gym=Gymnosperms

computing Specific Affiliation Index (SAI) following the large number of families and orders, but the affinity is not method of Rathore and Tiwari (2016). Species:family ratios as strong as in case of others. were also calculated as an indicative of nematode Hutchinson (1973) grouped all angiosperms families preference. in 111 orders on ascending evolutionary scale of which: 1- RESULTS AND DISCUSSION 54 placed in lignosae, 55-82 in herbaceae and 83-111 in monocotyledons (calyciferae 83-94; corolliferae 95-108; Results presented in Table 1 revealed that X. glumiflorae 109-111). Host range pattern showed that americanum selected 72.52% plants from dicotyledons and nematode feeds on diverse group of plants from 30 orders 17.57 and 9.91% from monocotyledons and gymnosperms, belonging to lignosae and 12 from herbaceae comprising respectively. Among the dicotyledons, plants from lignosae large number of families. Table 2 showed that host plants (fundamentally woody plants) were preferred to the tune of from families in dicotyledons were accepted from very 58.11% and less than 15% from herbaceae (fundamentally primitive orders like Magnoliales and Laurales in lignosae herbaceous plants). In monocotyledons, glumiflores were and Ranales in herbaceae. According to Hutchinson (1973) the best choice than plants from other categories. Magnoliales and Ranales evolved parallaly because Gymnosperms alone contributed substantial number of primitive families like Magnoliaceae in order Magnoliales plant species in the host range of this nematode.Value of and Paeoniaceae in order Ranales have some link between Specific Affiliation Index was highest for glumiflorae (1.250) them. On evolutionary scale Magnoliales and Laurales followed by gymnosperms (1.091) and lignosae (0.829). In occupied 1st and 3rd place in lignosae and Ranales 55th in spite of having higher percentage of plant species in herbaceae (most primitive in this group).However, in both lignosae the SAI was quite low, because plants in lignosae categories plants were parasitized from primitive to utilized more genera, species and orders than glumiflorae advanced orders. If we look into the evolutionary pattern and gymnosperms. This fact was further substantiated by in lignosae, Magnoliales via gave three basic species:family ratio, which was 3.07 in lignosae, 4.40 in stocks of plant orders viz., Rosales, Theales and Bixales gymnosperms and 23.00 in glumiflorae. Information, and each of these stocks possess 14, 3, 32 orders in their therefore, clearly indicates that though the nematode group, respectively. Rosales is a prolific stock and parasitized more plants in lignosae, which spread out in contributed 54.20% plants while Theales and Bixale stocks 5288 Trends in Biosciences 10 (25), 2017

Table 3. Distribution of host species in different taxonomic groups in APG IV system

Taxonomic groups Host species Genera Families Orders SAI Magnolids 4 ( 1.80) 3 ( 1.88) 2 ( 2.90) 2 ( 5.41) 0.857 Monocots 39 (17.57) 32 (20.00) 11 (15.94) 6 (16.22) 0.837 Eudicots 3 ( 1.35) 3 ( 1.88) 3 ( 4.35) 2 ( 5.41) 0,625 Superrosids 4 ( 1.80) 4 ( 2.50) 4 ( 5.80) 1 ( 2.70) 0.667 Rosids 92 (41.44) 56 (35.00) 21 (30.43) 10 (27.03) 1.08 Superasterids 5 ( 2.25) 5 ( 3.13) 4 ( 5.80) 1 ( 2.73) 0,700 Asterids 48 (21.62) 40 (25.00) 16 (23.19) 10 (27.03) 0.758 COM clade 5 ( 2.25) 4 ( 2.50) 3 ( 4.35) 1 ( 2.70) 0.875 Gymnospeerms 22 ( 9,91) 13 ( 8.13) 5 ( 7.25) 4 (10.81) 1.091 Figures in parentheses are % values

6.98 and 35.66% plants, respectively. The less advanced nematode parasitizing plants from primitive families in any orders like Rosales (6th position) and Leguminales (7th of the primitive orders. Liliales stock was byfar the position) contributed highest number of plants in lignosae most productive and contributed 35 host species. , whereas advanced order Asterales (76th position) in stock had four host species spreading in four herbaceae. In monocotyledons, there is no report of families. It also parasitized large number of plants from order

Table 4. Affiliation of host species to different taxonomic groups in APG IV system

Host spp. Taxonomic groups Families and orders (No.) Laurales: Lauraceae (3) 3 Magnolids Magnoliales: Magnoliaceae (1) 1

Asparagales: Amaryllidaceae (2), Asparagaraceae (2),Iridaceae (2) 6

Alismatales: Araceae (4) 4 Monocots Arecales: Arecaceae (1) 1 Zingiberales: Cannaceae (1), Musaceae (1), Srelitziaceae(1),Zingiberaceae (1) 4 Liliales: Liliaceae (1) 1 : Poaceae (23) 23 Buxales: Buxaceae (1) 1 Eudicots Proteales: (1), Proteaceae (1) 2

Superrosids Saxifragales: Crassulaceae (1), Hamamelidaceae (1),Paeoniaceae (1), Saxifragaceae (1) 4

Sapindales: Anacardiaceae (3), Rutaceae (6), Sapindaceae (2) 11 : Begoniaceae (1), Cucurbitaceae (2) 3 Brassicales: Brassicaceae (2) 2

Rosales: Elaeagnaceae (1), Moraceae (5), Rhamnaceae(1), Rosaceae (25), Ulmaceae (3) 35

Rosids Fabales: Fabaceae (17) 17 Fagales: (1), Fagaceae (4), Juglandaceae (3) 8 Geraniales: Geraniaceae (1) 1 Malvales: Malvaceae (3) 3 Myrtales: Lythraceae (1), Myrtaceae (3), Onagraceae (1) 5 Vitales: Vitaceae (7) 7

Superasterids Caryophyllales: (1), Amaranthaceae (2),Cactaceae (1), Nyctaginaceae (1) 5

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Host spp. Taxonomic groups Families and orders (No.) Apiales: Apiaceae (1), Araliaceae (3) 4 : Apocynaceae (2), Rubiaceae (1) 3 Aquifoliales: Aquifoliaceae (1) 1 Asterales: Asteraceae (12) 12 Dipsacales: Caprifoliaceae (2) 2 Asterids Solanales: Convolvulaceae (1), Solanaceae (4) 5 Ericales: Ebenaceae (1), Ericaceae (7), Theaceae (2) 10 Escalloniales: Escalloniaceae (1) 1 Cornales: Hydrangeaceae (1) 1 Lamiales: Lamiaceae (3), Oleaceae (6) 9 COM clade : Euphorbiaceae (1), Passifloraceae (1), Salicaceae (3) 5

Pinales. Leguminales (now Fabales) derived from Rosales stock Adoption of new system APG IV revealed not only (now also Rosales) and this supports the present findings. the newer way of presentation but placement of families Hutchinson (1973) described phylogenetic relationships and orders in different clades based on the analysis of as follows: chloroplast and ribosomal coding genes in association with Magnoliales—Dilleniales—Rosales——Leguminales morphological characters. In this system seven families of From both the systems, it also appears that nematode Hutchinson (1973) system were either merged or renamed. is furthering co-evolution with Asteraceae and Oleaceae as For example, Agavaceae—Asparagaceae, they share 37.50% plants in Asterids. Caesalpiniaceae— Fabaceae, Chenopodiaceae— Amaranthaceae, Corylaceae—Betulaceae, Dipsacaceae— ACKNOWLEDGMENTS Caprifoliaceae, Punicaceae—Lythraceae and Tiliaceae— Author is grateful to Mr. Akhilesh Rathore to extend Malvaceae. However, according to Cronquest system (1981) all possible help in retrieving the information. Tiliaceae can be separated from Malvaceae (sensu stricto) LITERATURE CITED by smooth surface of pollen grains, binocular anthers and the stamens free or in bundles. CABI 2013. Datasheets for plant parasitic nematodes Xiphinema americanum..CABI Crop Protection Compendium, Wallingford, In APG IV system of classification host plants U.K. grouped in 33 orders and 64 families and formed eight clades Cohn, E. 1970.Observations on the feeding and symptomology of (Table 3 and 4). According to this system, maximum number Xiphinema longidorus on selected host roots. Journal of of plants (41.44%) in Rosids followed by Asterids (21.62%) Nematology,2: 167-173. and Monocot (17.57%) and then followed by gymnosperms Christie, J.R. 1959. Plant nematodes, their bionomics and (9.91%). SAI were higher in gymnosperm (1.091), followed control.University of Florida Press. Agri. Exp. Stn., University by Rosids (1.080). Species:family ratio was maximum in of Florida, Gainsville, 256 p. gymnosperm (4.40), followed by Rosids (4.38) and monocots Cronquest, A. 1981.An integrated system of classification of flowering (3.345). Both these parameters elucidate that among plants. New York, Columbia University Press. angiosperms Rosids the most preferred group of plants Ferris, H. 2011. Nemabase Host Range of Genus and Species of followed by monocot (Table 3). Plant-feeding Nematodes.Retrieved 201-10-21. The most contributory families in the host range of Hockland, S. and Prior, T. 2009.Xiphinema americanum the nematode in Rosids are Fabaceae and Rosaceae, in sensulato.PM7/95 (1). EPPO Bulletin 39; 382-392. Monocots Poaceae and in gymnosperms Pinaceae. Hutchinson, J. 1973. Families of flowering plants.3rd ed., Oxford at Combined contribution of Fabaceae and Rosaceae was the Clarendon Press, 968 p. 56.52% plants in Rossids, Poaceae 58.97% plants in IPPC 2016. International Plant Protection Convention, ISPM 29- Monocots and Pinaceae 86.36% plants in gymnosperms. Diagonostic Prohibition of Regulated Pests, D.P. II: Xiphinema Collectively the aforesaid four families contributed 42.34% americanum sensulato, 19-26 pp. plants (94/222) of the total plant parasitized by this Jones, J.T., Haegeman, A., Etienne, G.J.D., Hari, S.G., Helder, J., nematode (Table 3). The information obtained from both Michael, G.K.J., Kikuchi, T., Rosa, M.L., Juan, E.P.R., Wesemael, the systems (Hutchinson, 1973 and APG IV) provides strong W.M.L. and Perry, R.W. 2013 Top 10 plant parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 4: signals that X. americanum co-evolved with plants in four 946-961. families, perhaps in different ecological niches or geographical regions and they are confamilial in their Lordello, L.G.E. 1972. Nematode pests of coffee. Pp. 409-434. In: Economic Nematology. J.M. Websrer (ed.), Academic Press, relationships.Hutchinson (1973) was of the view that 5290 Trends in Biosciences 10 (25), 2017

New York, 563 p. Rathore, Y.S. and Tiwari, S.N. 2016. Relationships of different Nemaplex 2017.Nemabase host range of genus and species of plant species of root-knot nematodes to their host taxonomic -feeding nematodes. Retrieved April, 2017. groupings. Intl. J. Plant, Animal and Environmental Sci., 7(1): 29-36. Norton, D.C. and Hoffman, J.K. 1974. Distribution of selected plant parasitic nematodes relative to vegetation and edaphic Rathore, Y.S. and Tiwari, S.N. 2016a. Host affinity of nematode factors. Journal of Nematology 6(2): 81-86. species of the genus Aphelenchoides. Intl. J. Sci. and Res., 5(9): 227-230. Rathore, Y.S. and Ali, S.S. 2014. Relationships of root-knot nematode, Meloidogyne incognita, with taxonomic groupings Robbinson, R.T. 1993. Distribution of Xiphinema americanum and of host plants. Trend in Bioscience, 7(13): 1562-1568. related species on North America. Journal of Nematoloy, 25(3): 344-348. Rathore, Y.S. and Tiwari, S.N. 2015. Relationships of different species of Heterodera with taxonomic groupings of host plants. Intl. J. Tarja, A.C. 1969. Variation within Xiphinema americanum group Plant Sci. Res, 4(7): 2269-2276. (Nematoda; Longidoridae).Nematologia, 15: 241-252. Rathore, Y.S. and Tiwari, S.N. 2015a. Relationships of species of White, L.V. 1955. Xiphinema americanum Cobb: its relationship to Helicotylenchus and taxonomic grouping of host plants. Intl. J. certain perennial crops. M.S. Thesis, Univ. Ark..Fayettevilla, Plant Sci. Res., 3(1): 1-7. Ark. Rathore, Y.S. and Tiwari, S.N. 2015b. Affinity of the species of Wikipedia 2017.APG IV system 9https://en.wikipedia.org/wiki/ Paratylechus (Tylenchida: Paratylenchidae) Intl. J. Sci. and APG_IV_system) Retrieved April 17, 2017. Res., 5(3): 1260-1263. Wikipedia 2017a. Xiphinema americanum (https://en.wikipedia.org/ wiki/xiphinema_americanum)

Received on 18-06-2017 Accepted on 25-06-2017