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First report of barley root-knot nematode, Meloidogyne naasi from turfgrass in Idaho, with multigene molecular characterization

Andrea M. Skantar

Andrea M. Skantar

Mycology and Nematology Genetic Diversity and Biology Laboratory, USDA, ARSBeltsville, USA
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Skantar, Andrea M.
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Zafar A. Handoo

Zafar A. Handoo

Mycology and Nematology Genetic Diversity and Biology Laboratory, USDA, ARSBeltsville, USA
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Handoo, Zafar A.
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Mihail R. Kantor

Mihail R. Kantor

Department of Plant Pathology and Environmental Microbiology, Pennsylvania State UniversityUniversity Park, USA
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Kantor, Mihail R.
 and 
Maria N. Hult

Maria N. Hult

Mycology and Nematology Genetic Diversity and Biology Laboratory, USDA, ARSBeltsville, USA
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Hult, Maria N.
  
Nov 20, 2023
First report of barley root-knot nematode, Meloidogyne naasi from turfgrass in Idaho, with multigene molecular characterization's Cover Image
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Article Category: Research Paper
Published Online: Nov 20, 2023
Received: Jun 28, 2023
DOI: https://doi.org/10.2478/jofnem-2023-0051
Keywords
© 2023 Andrea M. Skantar et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Figure 1:

Damage on golf course turfgrass in Banbury, Idaho. A. Golf course green in decline, showing patchy surface. B. Close-up of damage to mixed turfgrass, associated with M. naasi. Photo credits: Darryl Glinski.
Damage on golf course turfgrass in Banbury, Idaho. A. Golf course green in decline, showing patchy surface. B. Close-up of damage to mixed turfgrass, associated with M. naasi. Photo credits: Darryl Glinski.

Figure 2:

Photomicrographs of Meloidogyne naasi second-stage juveniles. A,B, heads; C, lateral lines; D,E, tails; the scale bar =10 μm.
Photomicrographs of Meloidogyne naasi second-stage juveniles. A,B, heads; C, lateral lines; D,E, tails; the scale bar =10 μm.

Figure 3:

Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 735-bp alignment of 28S rDNA sequences, with M. artiellia as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font.
Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 735-bp alignment of 28S rDNA sequences, with M. artiellia as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font.

Figure 4:

Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 1764-bp alignment of IGS-2 rDNA sequences, with M. hapla as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font.
Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 1764-bp alignment of IGS-2 rDNA sequences, with M. hapla as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font.

Figure 5:

Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 1764-bp alignment of mitochondrial sequences including the interval from COII to 16S, with M. hapla as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in bold font; other M. naasi is in blue and M. minor in red font.
Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 1764-bp alignment of mitochondrial sequences including the interval from COII to 16S, with M. hapla as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in bold font; other M. naasi is in blue and M. minor in red font.

Figure 6:

Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 763-bp alignment of mitochondrial COI sequences, with M. artiellia as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font. The COI sequence from Powers et al. (2018) is marked by an asterisk.
Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 763-bp alignment of mitochondrial COI sequences, with M. artiellia as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font. The COI sequence from Powers et al. (2018) is marked by an asterisk.

Figure 7:

Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 1003-bp alignment of Hsp90 genomic sequences, with M. hapla as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font.
Phylogenetic relationships of Idaho population of Meloidogyne naasi and other selected root-knot nematodes, as inferred from a 1003-bp alignment of Hsp90 genomic sequences, with M. hapla as the outgroup. A 50% majority rule consensus tree obtained from Bayesian analysis was generated using the GTR + I + G model of nucleotide substitution. Branch support (PP) values above 0.5 are shown on appropriate branches. New sequences are highlighted in blue bold font.

Root knot nematode isolates and GenBank numbers included in this study_

Species Origin Sample ID 28S IGS-2 mtCOI COII-16S Hsp90
M. arenaria Florida, USA - EU364880
Maryland, USA - FJ238508
Sri Lanka - MT741790
M. artiellia - - KY433447
- - KU517173
Italy - AY150369
M. chitwoodi - NEMBAR210 KU517168
Elko Co., Nevada, USA N7145 MH128483
N7147 MH128484
N7148 MH128485
N7149 MH128486
San Juan Co., NM P221087 MH128518
San Luis Obispo Co, CA 186 JN019321
USA JQ041535
Washington, USA P21040 MH128515
P215031 MH128516
P215032 MH128517
13B KC262220 (cl 1219)
KC262221 (cl 1220)
KC262222 (cl 1221)
KC262223 (cl 1222)
KC262224 (cl 1223)
M. christei Florida, USA - KR082317
M. dunensis Spain EF612712
M. enterolobii China HQ896361
Florida, USA 03A1 MH636612 (cl. 842)
M. exigua Brazil - AF435795
Nicaragua - HQ709105
N213 MH128476
N214 MH128477
N215 MH128478
M. fallax Netherlands* LW JN241952 (cl 2584) KC262225 (cl 2735)
KC262226 (cl 2736)
KC262227 (cl 2734)
KC262228 (cl 2737)
CA, USA 853 KC262229
KC262233
San Francisco Co., CA 853 KC241969 KC262260–KC262263
Scotland, United Kingdom P192084 MH128507
Switzerland - GQ395584
- NEMBAR256 KU517169
United Kingdom NEMBAR1145 KU517179
NEMBAR1174 KU517180
NEMBAR1180 KU517181
- KU517182
M. floridensis Peach Co., Georgia, USA Mf1 EU364884
Mf3 EU364885
Mf_GA2 EU364887
Mf_GA3 EU364888
M. graminicola China KY250093
MG917042–MG917045
- KM111533
Florida, USA P169011 MH128475
Phillippines HG529223
Taiwan KJ728847
Vietnam MH332671
Vietnam MH332672
M. graminis San Diego, Co., CA 730 JN019331
M. hapla China MW228371
Hawaii, USA AY52841
Maryland, USA*** (culture) AY528417
AF201338
Netherlands 7J2 KM491210
Netherlands DQ145641
Switzerland 6C1 KM491209
Qujing County, China MK359810
M. javanica Japan KF880398
Maricopa Co., Arizona, USA 001 JN019333
M. mali - NEMBAR1327 KU517178
M. marylandi King Co., Washington, USA 438 JN019324
M. minor Netherlands* LW 68D KC262259 JN241933 (cl 2636) KC262234 (cl. 2758)
JN241934 (cl 2638) KC262235 (cl. 2759)
JN241938 (cl 2640) KC262236 (cl. 2760)
JN241930 (cl 2641) KC262237 (cl. 2761)
Northern Ireland, United Kingdom* 202 KC262256 JN241940 (cl 2618) KC262242 (cl 2746)
JN241935 (cl 2619)
JN241942 (cl 2620)
JN241941 (cl 2621)
Northern Ireland, United Kingdom* 203 KC262257 JN241931 (cl 2624)
JN241942 (cl 2625)
JN241937 (cl 2627)
Northern Ireland, United Kingdom* 204 KC262258 JN241928 (cl 2633) KC262238 (cl 2748)
JN241932 (cl 2634) KC262239 (cl 2749)
JN241936 (cl 2635) KC262240 (cl 2751)
KC262241 (cl 2750)
- NEMBAR070 KU517170
M. naasi Ada Co., Idaho, USA 111B1 MT406252 OQ721995 MT408951 MT408947 (cl 3870)
111B2 OQ721994 MT408952 MT408952 MT408948 (cl 3872)
111B3 OQ721996 MT408953 MT408953 MT408949 (cl 3874)
MT408950 (cl 3875)
Idaho, USA** N326 MH128479
Jackson Co, Oregon, USA 410 JN019305
Lane Co., Oregon, USA 054 JN241903
Kitsap Co., Washington, USA 351 JN019316
King Co., Washington, USA 194 OQ721998
Linn Co., Oregon, USA 12A KM491211
KM491212
Linn Co., Oregon, USA 010
Monterey Co., California, USA 707
Stanislaus Co., California, USA 263
San Luis Obispo, Co., California, USA 163
San Diego Co., CA
Linn Co., Oregon, USA 12A KM491214
Monterey Co., California, USA 010 JN241909 KC262247 (cl 1229)
Stanislaus Co., California, USA 707 KC262248 (cl 1230)
San Luis Obispo, Co., California, USA 263 KC262249 (cl 1234)
San Diego Co., CA 163 KC262250 (cl 1232)
Reading, UK* 205 KC262251 (cl 1231)
KC262252 (cl 1233)
JN241897
JN241899
JN241910
JN241913
KM491213
Reading, UK* 205 KM491215
San Francisco Co., CA 79G3
Reading, UK* 205 JN241944 (cl 2541)
San Francisco Co., CA 79G3 KM491208
Sanpete Co, UT P199069 MH128480
Sanpete Co, UT P199071 MH128481
Sanpete Co, UT P199072 MH128482
Santa Clara Co., CA 245 OQ721997 JN241912
OQ721999
Van Buren Co., MI MG821326
Costa Rica KY962665
M. natalei Spain - EU570214
M. salasi Morocco - KP896293
M. silvestri Netherlands AF435801
M. spartelensis OR (garlic mustard) 95F5 MH590652 (cl 3255)
MH590653 (cl 3256)
95F6 MH590654 (cl 3260)
MH590655 (cl 3261)
MH590656 (cl 3262)
MH590657 (cl 3263)
M. trifoliophila
Meloidogyne sp.

Morphometrics of infective second-stage juveniles of Meloidogyne naasi_ Values expressed in the form mean +/− standard deviation (range)_

Characters Idaho Second-stage juveniles (n = 30) M. naasi (Franklin, 1965) (n = 25) M. naasi (Karssen et al., 2002) (n = 4) M. naasi (Zhao et al., 2017) (n = 17)
Linear (μm)
  Body length 427.9 ±16.73 (390 – 460) 435 (418 – 465) 421 ± 8.1 (410 – 429) 429 ± 16.1 (397 – 467)
  Maximum body width 16.2 (15.0 – 17.5)* 15 ± 0.95 (14 – 17.5) 14.1 ± 0.6 (13.3 – 14.5) 15.9 ± 0.7 (14.4 – 17.3)
  Stylet length 12.09 ± 0.56 (11.0 – 13.0) 14 (13 – 15) 13.3 ± 0.5 (12.6 – 13.9) 11.7 ± 0.6 (10.8 –1 2.4)
  Body width at anus 10.3 ± 0.9 (9.0 – 12.0)* 11 (9 –13) - -
  Tail length 70.3 ± 5.04 (62.0 – 80.0) 70 (52 – 78) 66.0 ± 3.9 (61.0 –70.0) 68.2 ± 8.0 (55–78)
  Hyaline tail terminus length 21.4 ± 2.16 (17.0 – 26.0) n.d. 17.9 ± 1.8 (15.8 – 19.6) 24.7 ± 2.6 (19.6 – 29.8)
  Lines in lateral field 4 4 - -
Ratios
  a = body length/greatest body diameter 35.61 ± 2.21 (32.24 – 40.91) 28 (25 – 32) 30 ± 1.5 (28.3 – 31.8) 27.1 ± 1.9 (24.2 – 30.7)
  c = body length/tail length 6.11 ± 0.43 (4.94 – 6.79) 6.2 (n.d.) 6.4 ± 0.3 (6.0 – 6.7) 6.4 ± 0.8 (5.6 – 8.0)
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