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.
Table 1:
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) |
Figure 2:
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.
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.
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.
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.
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.
Supplementary Table S1.
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. |