Brown root rot caused by phellinus noxius in the Ogasawara(Bonin) islands, southern Japan - current status of the diseaseand its host plants

Norio Sahashi1 & Mitsuteru Akiba1 & Yuko Ota1 & Hayato Masuya2 & Tsutomu Hattori1 &

Akitsugu Mukai3 & Ritsuko Shimada3 & Tsuyoshi Ono4 & Toyozo Sato5

Received: 5 June 2015 /Accepted: 29 October 2015 /Published online: 3 November 2015# Australasian Plant Pathology Society Inc. 2015

Abstract An unusual mortality of several woody plant spe-cies was recently found in the Ogasawara Islands. Here, weshow that brown root rot caused by Phellinus noxius was theprimary cause of this unusual tree death. Typical symptoms ofthe disease were confirmed on 41 plant species in 29 plantfamilies. Among them, 23 were novel hosts of P. noxius, in-cluding 15 species endemic to the Ogasawara Islands. Sixspecies were new host records in Japan.

Keywords Brownroot rot .Phellinusnoxius .TheOgasawaraislands . Host plants

Phellinus noxius is widespread among tropical and sub-tropical regions throughout the world, where it causes brown

root rot disease in a variety of woody tree species (Ann et al.1999, 2002; Bolland 1984; Brooks 2002; CABI/EPPO 1997;Chang 1995; Chang and Yang 1998; Hodges and Tenorio1984; Ivory 1996; Larsen and Cobb-Poule 1990; Nandriset al. 1987; Neil 1986). Affected trees show reduced growth,leaf discoloration, wilting, defoliation, and branch dieback,and most eventually die (Sahashi et al. 2012, 2014). The fun-gus has a broad host range (Ann et al. 2002; Bolland1 984;Ivory 1996) with little host specificity (Ann et al. 1999; Chang1995; Sahashi et al. 2010).

In Japan, brown root rot was first found on IshigakiIsland, Okinawa Prefecture in 1988 (Abe et al. 1995). Sincethen, the disease has been reported on many islands, causingserious problems in subtropical regions of southern Japan(Sahashi et al. 2012).

The Ogasawara Islands are oceanic islands located approx-imately 1000 km south of Tokyo (Fig. 1). Phellinus noxiuswas suspected of causing the disease on the Islands becausethe fruiting body of the fungus, but not the disease was alreadyfound there (Yasuda 1916) and the climate and plant speciescomposition are similar to those on the Ryukyu Islands.Recently, one of the authors noticed the unusually high mor-tality of several woody plant species along roads on theIslands. To identify the cause, we conducted several field sur-veys from 2011 to 2013 on the two main islands, Chichijimaand Hahajima (Fig. 1). We also carried out small surveys ontwo uninhabited islands (Anijima and Otoutojima). During thesurveys, we evaluated all declining or dead trees that could beobserved from roads (including forest roads) and recreationaltrails in sightseeing areas throughout each of the islands, es-pecially the two main islands. In addition, we examined some

* Norio Sahashisahasi@affrc.go.jp

1 Department of Forest Microbiology, Forestry and Forest ProductsResearch Institute (FFPRI), Matsunosato 1, Tsukuba 305-8687,Japan

2 Tohoku Research Center, FFPRI, Morioka 020-0123, Japan3 Greenery Environment Section, Ogasawara Branch of Tokyo

Metropolitan Government, Aza-Nishimachi, Chichijima 100-2101,Japan

4 Agro-Environment Division, Tokyo Metropolitan Agriculture andForestry Research Center, Fujimi-cho 3-8-1,Tachikawa, Tokyo 190-0013, Japan

5 Genetic Resources Center, National Institute of AgrobiologicalSciences, (NIAS), Kannonndai 2-1-2, Tsukuba 305-8602, Japan

Australasian Plant Dis. Notes (2015) 10: 33DOI 10.1007/s13314-015-0183-0

tree species grown in a glass greenhouse at OgasawaraSubtropical Agricultural Center of the Tokyo MetropolitanGovernment. When we found affected trees, we examinedthe roots and stem bases carefully for characteristic symptomsof the disease described in many studies (Ann et al. 2002;Hodges and Tenorio 1984; Ivory 1996; Sahashi et al. 2012).Tissue samples from roots and stem bases with typical symp-toms were returned to the laboratory for fungal isolation. Theisolation of fungi was conducted according to Sahashi et al.(2007). The identification of P. noxiuswas made based on thecharacteristics (e.g. colony morphology with irregular darkbrown patches; staghorn-like hyphae formation) of pure cul-tures on PDA (Sahashi et al. 2012) and molecular sequencesof the large subunit (LSU) of nuclear ribosomal DNA(rDNA). For molecular identification, we used two LSU data(DDBJ Accession Nos. LC049950 and LC049951) derivedfrom two P. noxius isolates (WD 1223 obtained from a fruitingbody and FFPRI 411142 obtained from a single basidiospore)as reference sequences. These isolates were identified asP. noxius by their morphological characters of fruiting bodies(Abe et al. 1995; Corner 1932). Then, representative isolates

including FFPRI 411142 collected from each of 38 differenttree species were chosen (Table 1), and the DNA sequences ofthe LSU of the isolates were compared with the P. noxiusreference sequences described above. Isolate FFPRI 411142was treated as a representative isolate because this was theonly isolate obtained from Melia azedarach var.subtripinnata. These isolates were deposited in FFPRIGenebank (FFPRI 11120–11,156) and NAIS Genebank(MAFF243592) (Table 1). All sequence data determined inthe present study were also deposited in the DDBJ(Accession Nos. LC066600 –066,636).

We found typical symptoms of brown root rot in 41 plantspecies in 29 plant families at 67 sites in all 4 islands surveyed(Fig. 1, Table 1). Phellinus noxius was isolated from almost allnewly dead or declining trees with disease symptoms. Wecould not isolate P. noxius from three plant species, but weconsidered that these species are host plants of P. noxius be-cause typical symptoms of brown root rot were observed onthese plants (Table 1). The LSU of rDNA (940 bp) from therepresentative isolates collected in this study showed 99.5–100 % similarities with the P. noxius reference sequence data

Otoutojiima Is.1 site

N140 0’0’’130 0’0’’

Anijima Is.

1 site

4 sites

Sea of Japan40 0’0’’

Tokyo

Pacific Ocean

30 0’0’’

Hahajima Isles

Chichijima Isles

Chichijima Is.

Hahajima Is.26 sites

36 sites

20 0’0’’

2km

Fig. 1 Geographic distribution ofbrown root rot on the OgasawaraIslands. Black dots indicate siteswhere brown root rot (or fruitingbody of Phellinus noxius) wasconfirmed

33 Page 2 of 5 Australasian Plant Dis. Notes (2015) 10: 33

Table 1 Host records of brown root rot caused by Phellinus noxius in the Ogasawara Islands, Japan

Plant family Plant species Isolation of P.noxius Representative isolate used

Anacardiaceae Mangifera indica a, c, d Yes FFPRI 411120

Spondias dulcis a, d Yes FFPRI 411121

Rhus succedanea, (Syn.Toxicodendron succedaneum ) Yes FFPRI 411122

Apocynaceae Ochrosia nakaiana b, e Yes FFPRI 411123

Trachelospermum asiaticum e Yes FFPRI 411124

Aquifoliaceae Ilex mertensii b,e Yes FFPRI 411125

Bombacaceae Pachira aquatica a, c, d, (Syn. P. macrocarpa ) Yes FFPRI 411126

Casarinaceae Casuarina equisetifolia a Yes FFPRI 411127

Celastracecae Euonymus boninensis b,e Yes FFPRI 411128

Clusiaceae Calophyllum inophyllum Yes FFPRI 411129

Combretaceae Terminalia catappa d Yes FFPRI 411130

Elaegnaceae Elaeagnus rotundata b, e Yes FFPRI 411131

Euphorbiaceae Jatropha integerrima a, c, (Syn. J. pandurifolia ) Yes FFPRI 411132

Bischofia javanica a Yes FFPRI 411133

Fabaceae (Leguminosae) Erythrina variegata a Yes MAFF 243592

Leucaena leucocephala a Yes FFPRI 411134

Hamamelidaceae Distylium lepidotum b, e Yes FFPRI 411135

Lauraceae Cinnamomum pseudopedunculatum b, e Yes FFPRI 411136

Machilus kobu b, e Yes FFPRI 411137

Neolitsea sericea e Yes FFPRI 411138

Malpighiaceae Malpighia emarginata a, c, e Yes FFPRI 411139

Malvaceae Hibiscus glaber b, e Yes FFPRI 411140

Meliaceae Melia azedarach var. subtripinnata Yes FFPRI 411141 f

Moraceae Ficus benghalensis a, e Yes FFPRI 411142

Ficus elastica a, d Yes FFPRI 411143

Morus australis Yes FFPRI 411144

Myrsinaceae Ardisia sieboldii Yes FFPRI 411145

Myrtaceae Psidium cattleianum f. lucidum a, e Yes FFPRI 411146

Oleaceae Ligustrum micranthum b, e Yes FFPRI 411147

Osmanthus insularis e Yes FFPRI 411148

Pandanaceae Pandanus boninensis b, e Yes FFPRI 411149

Rosaceae Cerasus campanulata , (Syn. Prunus cerasoides var. campanulata ) Yes FFPRI 411150

Rhaphiolepis indica var. umbellata Yes FFPRI 411151

Rubiaceae Hedyotis leptopetala b, e No

Rutaceae Zanthoxylum ailanthoides var. boninshimae b, e Yes FFPRI 411152

Sapotaceae Planchonella obovata e Yes FFPRI 411153

Theaceae Schima mertensiana b, e Yes FFPRI 411154

Thymelaeaceae Wikstroemia pseudoretusa b, e No

Ulmaceae Celtis boninensis Koidz. b, e Yes FFPRI 411155

Australasian Plant Dis. Notes (2015) 10: 33 Page 3 of 5 33

(DDBJAccession Nos. LC049950 and LC049951), supportingthat isolates collected in the present study are P. noxius. Amongthe 41 species, 23 were novel hosts of P. noxius, including 15

species endemic to the Ogasawara Islands, and 6were new hostrecords for Japan (Table 1).

There are a large number of valuable plants that are foundonly on the Ogasawara Islands (Toyoda 2014). As the patho-gen has a broad host range, it is possible that the damage willspread, further decreasing the population of these importanttree species. Therefore, it is necessary to sufficiently monitorthe expansion of the damage.

The diseased trees exhibited characteristic symptoms sim-ilar to those reported in other studies, including a dark brownmycelial crust at the stem base with a white creamy leadingedge (Fig. 2a-d), roots covered with a mycelial mat containingsoils (Fig. 2e, g), and white root rot with conspicuous brownlines (Fig. 2f, g), (Ann et al. 2002; Ivory 1996; Nandris et al.1987; Sahashi et al. 2012). Unlike the Ryukyu Islands, how-ever, encrustations extended more than 1 m above the groundas reported in many tropical areas (Brooks 2002; Ivory 1996;Hodges and Tenorio 1984).

The disease was often found in the areas associated withhuman activities, and was typically present in a number ofadjacent trees, creating infection centers (Fig. 3). These sug-gest that the pathogen was spreading via root-to-root contact,at least after the first infection occurred, as has been reported

Fig. 2 Characteristic symptoms of root and stem base infected withPhellinus noxius. (a- d) A dark brown to black mycelial crust at thestem base; encrustation sometimes grows up to over 1 m above theground. e A lateral root covered with a black mycelial mat withadhering soil particles and stones. f Well developed white rot withconspicuous brown lines permeating the rotted wood. g A fallen treewith a black mycelial crust on the stem and roots, and a typical whiterot containing brown lines

Fig. 3 Adisease focus (large gap) caused by brown root rot disease. Notethat several trees are dead or dying. The infection centers are sometimesup to ca. 400 m2 in size

Table 1 (continued)

Plant family Plant species Isolation of P.noxius Representative isolate used

Trema orientalis d Yes FFPRI 411156

Verbenaceae Stachytarpheta jamaicensis a, e No

a Introduced speciesb Ogasawara endemic speciesc These plants were grown in greenhousedNew host record in JapaneNew host record in the worldf Isolete from a single basidiospore

33 Page 4 of 5 Australasian Plant Dis. Notes (2015) 10: 33

in many countries (Ann et al. 2002; Bolland 1984; Hodgesand Tenorio 1984; Nandris et al. 1987; Sahashi et al. 2012;Singh et al. 1980).

Phellinus noxiuswas also found on dead and fallen trees innatural forests with little human disturbance, but spreading ofthe pathogen was limited to a few neighboring healthy trees,and therefore did not create large disease foci. It is unclearwhy the pathogen was not able to spread and induce diseasein this case. Fruiting bodies were rare in the field, but theywere found more frequently than in the Ryukyu Islands. Infact, mature fruiting bodies were sometimes observed on deadand/or fallen trees at several sites (Fig. 4). Some fruiting bod-ies were confirmed to be dispersing basidiospores by the na-ked eye, and also by capturing spores using glass slide coatedwith Vaseline put under fruiting bodies. These findings sug-gest that disease dispersal by basidiospores in the OgasawaraIslands might be occurring more frequently than in theRyukyu Islands.

Further studies on favorable conditions for disease occur-rence and effective control procedures should be undertakento reduce the damage from the disease.

Acknowledgments This study was financially supported in part by agrant-in-aid for scientific research to Y. O. (No. 25292096) from theJapan Society for the Promotion of Science and by a fund to T. H. pro-vided by Institute for Fermentation, Osaka. This study was undertakenwith permission from Forestry Agency, Ministry of Agriculture, Forestryand Fisheries, and Ministry of the Environment.

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