Mathematical modeling of positron emission tomography (PET) data to assess radiofluoride transport in living plants following petiolar administration

Plant Methods

Onofre T DeJesus¹  Paul H Williams²  Robert J Nickles¹  Todd E Barnhart¹  Jonathan W Engle¹  Paul A Ellison¹  Katherine A Lake¹  Jackson D Hetue²  Tom W Bryan²  Elizabeth O Ahlers³  Alexander K Converse³ 

[1] Department of Medical Physics, University of Wisconsin-Madison, Madison 53705, WI, USA;Department of Plant Pathology, University of Wisconsin-Madison, Madison 53705, WI, USA;T123 Waisman Center, University of Wisconsin-Madison, Madison 53705, WI, USA

关键词: Brassica oleracea;    Kinetic modeling;    Radiotracer;    Positron emission tomography;    Ion transport;   

Others  :  1174976
DOI  :  10.1186/s13007-015-0061-y

 received in 2014-11-04, accepted in 2015-02-25,  发布年份 2015

【 摘 要 】

Background

Ion transport is a fundamental physiological process that can be studied non-invasively in living plants with radiotracer imaging methods. Fluoride is a known phytotoxic pollutant and understanding its transport in plants after leaf absorption is of interest to those in agricultural areas near industrial sources of airborne fluoride. Here we report the novel use of a commercial, high-resolution, animal positron emission tomography (PET) scanner to trace a bolus of [¹⁸F]fluoride administered via bisected petioles of Brassica oleracea, an established model species, to simulate whole plant uptake of atmospheric fluoride. This methodology allows for the first time mathematical compartmental modeling of fluoride transport in the living plant. Radiotracer kinetics in the stem were described with a single-parameter free- and trapped-compartment model and mean arrival times at different stem positions were calculated from the free-compartment time-activity curves.

Results

After initiation of administration at the bisected leaf stalk, [¹⁸F] radioactivity climbed for approximately 10 minutes followed by rapid washout from the stem and equilibration within leaves. Kinetic modeling of transport in the stem yielded a trapping rate of 1.5 +/− 0.3%/min (mean +/− s.d., n = 3), velocity of 2.2 +/− 1.1 cm/min, and trapping fraction of 0.8 +/− 0.5%/cm.

Conclusion

Quantitative assessment of physiologically meaningful transport parameters of fluoride in living plants is possible using standard positron emission tomography in combination with petiolar radiotracer administration. Movement of free fluoride was observed to be consistent with bulk flow in xylem, namely a rapid and linear change in position with respect to time. Trapping, likely in the apoplast, was observed. Future applications of the methods described here include studies of transport of other ions and molecules of interest in plant physiology.

【 授权许可】

   
2015 Converse et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Assmann SM. From proton pump to proteome. Twenty-five years of research on ion transport in higher plants. Plant Physiol. 2001; 125:139-41.
• [2]Brouwer R. Ion absorption and transport in plants. Annu Rev Plant Physiol. 1965; 16:241-66.
• [3]Nardini A, Salleo S, Jansen S. More than just a vulnerable pipeline: xylem physiology in the light of ion-mediated regulation of plant water transport. J Exp Bot. 2011; 62:4701-18.
• [4]Minchin PEH, Thorpe MR. Using the short-lived isotope C-11 in mechanistic studies of photosynthate transport. Funct Plant Biol. 2003; 30:831-41.
• [5]Farwell MD, Pryma DA, Mankoff DA. PET/CT imaging in cancer: current applications and future directions. Cancer. 2014; 120(22):3433-45.
• [6]Bartlett RM, Dejesus OT, Barnhart TE, Nickles RJ, Christian BT, Graner JL et al.. Fetal dopamine receptor characteristics assessed in utero. J Cereb Blood Flow Metab. 2010; 30:1437-40.
• [7]Weinstein LH, Davison AW. Fluorides in the Environment: Effects on Plants and Animals. CABI Publishing, Wallingford, UK; Cambridge, MA; 2004.
• [8]Mesquita GL, Ossamu Tanaka FA, Cantarella H, Mattos D. Atmospheric absorption of fluoride by cultivated species. Leaf structural changes and plant growth. Water Air Soil Pollut. 2011; 219:143-56.
• [9]Groth E. Fluoride pollution. Environment. 1975; 17:29-38.
• [10]Baunthiyal M, Bhatt A, Ranghar S. Fluorides and its effects on plant metabolism. Int J Agric Technol. 2014; 10:1-27.
• [11]McKay RML, Palmer GR, Ma XP, Layzell DB, McKee BTA. The use of positron emission tomography for studies of long-distance transport in plants - uptake and transport of F-18. Plant Cell Environ. 1988; 11:851-61.
• [12]Kume T, Matsuhashi S, Shimazu M, Ito H, Fujimura T, Adachi K et al.. Uptake and transport of positron-emitting tracer (F-18) in plants. Appl Radiat Isot. 1997; 48:1035-43.
• [13]Nakanishi TM, Tanoi K, Yokota H, Kang DJ, Ishii R, Ishioka NS et al.. F-18 used as tracer to study water uptake and transport imaging of a cowpea plant. J Radioanal Nucl Chem. 2001; 249:503-7.
• [14]Converse AK, Ahlers EO, Williams PH, Engle JW, Barnhart TE, Nickles RJ, et al. Fluoride transport in brassica: a positron emission tomography botanical study [poster MIC9.S-1]. IEEE Nucl Sci Symp Med Imaging Conf Conf Rec. 2011.
• [15]Converse AK, Ahlers EO, Bryan TW, Williams PH, Barnhart TE, Engle JW et al.. Positron emission tomography (PET) of radiotracer uptake and distribution in living plants: methodological aspects. J Radioanal Nucl Chem. 2013; 297:241-6.
• [16]Keutgen N, Matsuhashi S, Mizuniwa C, Ito T, Fujimura T, Ishioka NS et al.. Transfer function analysis of positron-emitting tracer imaging system (PETIS) data. Appl Radiat Isot. 2002; 57:225-33.
• [17]Williams PH, Hill CB. Rapid-cycling populations of Brassica. Science. 1986; 232:1385-9.
• [18]Ohya T, Tanoi K, Hamada Y, Okabe H, Rai H, Hojo J et al.. An analysis of long-distance water transport in the soybean stem using H215O. Plant Cell Physiol. 2008; 49:718-29.
• [19]Lin Y-H, Lin M-H, Gresshoff PM, Ferguson BJ. An efficient petiole-feeding bioassay for introducing aqueous solutions into dicotyledonous plants. Nat Protoc. 2011; 6:36-45.
• [20]Alexoff DL, Dewey SL, Vaska P, Krishnamoorthy S, Ferrieri R, Schueller M et al.. PET imaging of thin objects: measuring the effects of positron range and partial-volume averaging in the leaf of Nicotiana tabacum. Nucl Med Biol. 2011; 38:191-200.
• [21]Bühler J, von Lieres E, Huber G. A class of compartmental models for long-distance tracer transport in plants. J Theor Biol. 2014; 341:131-42.
• [22]Ferrieri RA, Gray DW, Babst BA, Schueller MJ, Schlyer DJ, Thorpe MR et al.. Use of carbon-11 in Populus shows that exogenous jasmonic acid increases biosynthesis of isoprene from recently fixed carbon. Plant Cell Environ. 2005; 28:591-602.
• [23]Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR et al.. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci. 2014; 19:623-30.
• [24]Barnhart TE, Converse AK, Dabbs KA, Nickles RJ, Buckley K, Jivan S et al.. Water-cooled grid support for high-power irradiation with thin target windows. Appl Radiat Isot. 2003; 58:21-6.