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Xylem Dysfunction in Bursaphelenchus Xylophilus-Infected Pinus Thunbergii in Relation to Xylem Cavitation and Water Status

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Xylem Dysfunction in Bursaphelenchus Xylophilus-Infected Pinus Thunbergii in Relation to Xylem Cavitation and Water Status 日 植 病 報 62: 554-558 (1996) Ann. Phytopathol. Soc. Jpn. 62: 554-558 (1996) Xylem Dysfunction in Bursaphelenchus xylophilus-infected Pinus thunbergii in Relation to Xylem Cavitation and Water Status Takefumi IKEDA* Abstract The occurrence of cavitation in Bursaphelenchus xylophilus-inoculated Pinus thunbergii was evaluat- ed by analyzing acoustic emissions and water status in pine saplings. As determined from changes in the minimum xylem pressure potential, pine wilt disease development occurred in two stages. A small amount of cavitation occurred during the latter half of the first stage of disease development. As the infection progressed, cavitation increased. The occurrence of cavitation was greater after B. xylophilus inoculation when the xylem pressure potential was constant. The presence of B. xylophilus in pine increased the plant's potential for cavitation. In the second stage of disease development, a large increase in cavitations in the tracheids led to catastrophic destruction of the water conducting pathway. These findings support the idea of “runaway embolism” having a major role in mechanism of induction of pine wilt disease. (Received June 21, 1996; Accepted August 27, 1996) Key words: Bursaphelenchus xylophilus, cavitation, xylem embolism, pine wilt disease, Pinus thunbergii, water status. INTRODUCTION MATERIALS AND METHODS Xylem dysfunction is one of the most typical symp- Experimental materials and nematode inocula- toms in pines infected with Bursaphelenchus xylophilus tion. One four-year-old and two three-year-old (Steiner and Buhrer) Nickle, the pine wood nematode. Japanese black pine saplings were used in a glass house This symptom is characterized by a decrease in, and an study. Pine #1 was 158cm tall, pine #2 was 93cm tall, eventual loss of the water-conducting function of the and pine #3 was 89cm tall. The T4 virulent isolate of B. xylem3,4,7,9,11,13,18-20)which leads to the rapid wilting of xylophilus, which was collected from a dead Pinus pine wilt disease14). This disruption of water transport densiflora Sieb. et Zucc. at Morioka, Iwate Prefecture, influences water relations and other ecophysiological was grown on barley seed cultures of Botrytis cinerea features in plants. Xylem embolism, the major cause of Pars. and used to inoculate the saplings through a wound xylem dysfunction, results from cavitation in the water on the current shoot. This wound was made by a cut column of the tracheid21,23). Although several investiga- with a small saw and peeling back a short length of the tors have reported changes in water relations in B. bark. Experiments were done during the summer xylophilus-infected pines, the mechanism by which xylem months. dysfunction is induced in these pines is not fully under- Detection of acoustic emission (AE) and evalua- stood. tion of water status. Cavitation was monitored by Over the last decade major advances in understanding determining AE events using a PZT transducer, 8mm in tree water relations have elucidated the mechanism of diameter and 15mm in height with a peak sensitivity at xylem embolism caused by cavitation17,23). In this study 0.5MHz (AE 904US). An AE event was defined as counts I have evaluated xylem cavitation in B. xylophilus- measured over a 24-hour period beginning at 6:00 a.m. inoculated Pinus thunbergii Parl., (Japanese black pine) of one day and ending at 6:00 a.m. of the next day. This by analyzing acoustic emission of ultrasonic frequencies period included sunrise which was between 5:10 a.m. and have described the relationship between the occur- and 5:30 a.m. in the summer months when the experi- rence of cavitation and the water status of the pine. ments were done. The AE signals were amplified by 60 dB with an AE 912 preamplifier and an AE 922 dis- criminator with a bandpass filter of 0.1-1.0MHz. To count AE events, an AE 932 dual counter was used. All * Kansai Research Center , Forestry and Forest Products Research Institute, Fushimi, Kyoto 612, Japan 森 林 総 合 研 究 所 関 西 支 所 Ann. Phytopathol. Soc. Jpn. 62 (6). December, 1996 555 AE instruments were from NF Electronic Instruments, disease development occurred in two stages (Fig. 1). The Japan. The AE transducer was attached directly to the slight changes in water status, characteristic of the first xylem tissue at the site of wounding and sealed in place stage of the disease, were followed by an abrupt with petroleum jelly and covered with polyvinylidene decrease in minimum xylem pressure potential which chloride film and aluminum foil to prevent water loss characterized the second stage. This agreed well with and temperature increases at the xylem. Acoustic emis- the results from several other studies2,5,7,9). Xylem pres- sion activity was first detected in P. thunbergii in the sure potential decreased with a decrease in soil water morning when the xylem pressure potential of needle potential and AE events increased with a decrease in was -0.9 to -1.0MPa and xylem pressure potential xylem pressure potential in pine needles before peaked about midday8). Based on these parameters, the nematode inoculation (Fig. 1). Thus xylem pressure water status relative to the induction of cavitation was potential changes coincided well with changes in soil evaluated by measuring the minimum xylem pressure water potential. potential of current year needles at 1:00 p.m. This This correlation of xylem pressure potential to measurement was made with a pressure chamber (PMS changes in soil water potential continued through day 6 Instrument, USA). Soil water status was measured with after inoculation of pine #1, day 7 in pine #2 and day 5 in a mercury tensiometer at the same time. Air tempera- pine #3 indicating that, during the first half of the first ture, relative humidity, and photosynthetically active stage of disease development, the presence of the radiation (PAR) in the glass house were measured with nematode did not generate acoustic emission events. As a humidity/temperature probe (AKH 2013, Skye Instru- the first stage of pine wilt disease reached a conclusion, ment Ltd., UK) and a quantum sensor (Li 190S, Li-Cor, however, a small number of acoustic emission events USA). Acoustic emission counts and temperature, were recorded. As the second stage of disease develop- humidity, and PAR data were collected at one hour ment began, xylem pressure potentials abruptly de- intervals and stored in a data logger (LI-1000, Li-Cor, creased and a large number of acoustic emissions were USA) throughout the study. generated. This occurred at day 19 after inoculation in The reduction and cessation of oleoresin exudation, pine #1, day 10 in pine #2 and day 11 in pine #3. This the first detectable internal symptoms of pine wilt dis- great increase in AE events was followed by a sudden ease, were quantitatively evaluated by measuring the decrease in xylem pressure potential until no events amount of resin which accumulated after several hours could be recorded, indicating that all tracheids had at a wound, made by drilled a hole with a small gimlet cavitated and that all xylem possessed an embolism that through the bark and into the sapwood. completely inhibited water conduction in the xylem. Acoustic emission events on days 7, 11, 13, and 14 after RESULTS AND DISCUSSION inoculation of pine #1, day 8 in pine #2 and on days 6 and 7 after inoculation in pine #3 were greater than those All B. xylophilus-inoculated pine died. Pine wood measured at a similar xylem pressure potential before nematodes were recovered from these pines. inoculation and during the first half of the first stage of As determined from changes in water status based on disease development (Fig. 2). This indicates that the minimum xylem pressure potential differences, pine wilt relationship of AE events to xylem pressure potential Fig. 1. (a) Soil water potential (SWP) in pot soil, and (b) AE (acoustic emission) rate (○) and minimum xylem pressure potential (●) of pine needle in Pinus thunbergii before and after inoculation with Bursaphelenchus xylophilus. Arrows show the cessation of resin flow. I and II in (b) show the first and second stage of disease development, respectively. 556 日本植物病理学会報 第62巻 第6号 平成8年12月 Fig. 2. Relationship between AE (acoustic emission) rate at the same of xylem pressure potential before and after inoculation with B. xylophilus in pine #1, #2 and #3. ○ and ●, before and after inoculation in pine #1; △ and ▲, before and after inoculation in pine #2; □ and ■, before and after inoculation in pine #3. Fig. 3. Diurnal trends in (a) acoustic emissions (AE) and (b) photosynthetically active radiation (PAR) (○) and vapor pressure deficit (VPD) (●) five days before and 10 days after inoculation with B. xylophilus in pine #2. before inoculation and during the early part of the first in B. xylophilus-inoculated Japanese black pine result stage of disease development is much different than that from the rise and fall in water tension induced by the late in the first stage. Because cavitation is dependent on concomitant increase and decrease in transpiration. the strength of water tension, this study shows that During the initial phases of pine wilt disease develop- cavitation occurred more easily after inoculation than ment in B. xylophilus-infected Japanese black pine, before inoculation when water tension was the same. water status changes very little, even though xylem Based on recent studies by Pockman et al.17) and by hydraulic conductance has already decreased9). By the Tyree and Sperry23), this facilitation of cavitation in B. end of the first stage of pine wilt disease, xylem hydrau- xylophilus-infected pine may be the result of modifica- lic conductance is reduced to 20 to 40 percent of the level tions of surface tension of water in the tracheids and/or in non-infected trees9).
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