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Phosphate Status Affects Phosphate Transporter Expression and Glyphosate Uptake and Transport in Grand Eucalyptus (Eucalyptus grandis)

Published online by Cambridge University Press:  03 October 2018

Fernanda Campos Mastrotti Pereira
Affiliation:
Doctoral Student, Department of Applied Biology to Agropecuary, São Paulo State University, Jaboticabal, Brasil; and Department of Environmental Science and Technology, University of Maryland, College Park, MD, USA
Reuben Tayengwa
Affiliation:
Postdoctoral Fellow, Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD, USA
Pedro Luis Da Costa Aguiar Alves
Affiliation:
Professor, Department of Applied Biology to Agropecuary, São Paulo State University, Jaboticabal, Brasil
Wendy Ann Peer*
Affiliation:
Assistant Professor, Department of Environmental Science and Technology, University of Maryland, College Park, MD, USA; and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD, USA; and Institute for Bioscience and Biotechnology Research, University of Maryland, College Park, MD, USA
*
Author for correspondence: W. A. Peer, Department of Environmental Science and Technology, University of Maryland, College Park, MD 20742. (Email: wapeer@umd.edu)

Abstract

Soluble phosphate availability is a major limiting factor for plant growth, development, and yield. To assure a constant phosphorous supply, plants employ both high- and low-affinity phosphate acquisition mechanisms. Glyphosate is an herbicide widely used throughout the world, and previous studies have suggested that it can be transported across the plasma membrane via phosphate transporters in herbaceous species. The effects of phosphate status on glyphosate uptake were investigated in the tree grand eucalyptus (Eucalyptus grandis W. Hill ex. Maid.). Eucalyptus grandis’s putative phosphate transporters showed differential gene expression in leaves and roots in response to phosphate limitation. Overall, the expression of high-affinity phosphate transporters increased in phosphate-limiting treatments, particularly in roots. More [14C]glyphosate was absorbed and translocated in phosphate-limiting plants compared with control plants grown in phosphate-replete treatments. In leaf mesophyll protoplast assays, rapid uptake of [14C]glyphosate into protoplasts was observed, and addition of phosphate to the assays competed with [14C]glyphosate uptake. These data indicate that phosphate transporters represent one mechanism of glyphosate uptake in E. grandis. These results have implications for best management practices for weed control and glyphosate application under phosphate application regimes.

Type
Research Article
Copyright
© Weed Science Society of America, 2018 

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References

Ai, P, Sun, S, Zhao, J, Fan, X, Xin, W, Guo, Q, Yu, L, Shen, Q, Wu, P, Miller, AJ, Xu, G (2009) Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J 57:798809 Google Scholar
Arabidopsis Genome Initiative, (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana . Nature 408:796815 Google Scholar
Arpat, AB, Magliano, P, Wege, S, Rouached, H, Stefanovic, A, Poirier, Y (2012) Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. Plant J 71:479491 Google Scholar
Barja, BC, Herszage, J, Dos Santos Afonso, M (2001) Iron(III)–phosphonate complexes. Polyhedron 20:18211830 Google Scholar
Bott, S, Tesfamariam, T, Kania, A, Eman, B, Aslan, N. Romheld, V, Neumann, G (2011) Phytotoxicity of glyphosate soil residues re-mobilised by phosphate fertilization. Plant Soil 342:249263 Google Scholar
Bustin, SA, Benes, V, Garson, JA, Hellemans, J, Huggett, J, Kubista, M, Mueller, R, Nolan, T, Pfaffl, MW, Shipley, GL, Wittwer, CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Chin J Chem 48:11781185 Google Scholar
Calderon-Vazquez, C, Ibarra-Laclette, E, Caballero-Perez, J, Herrera-Estrella, L (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant and species-specific levels. J Exp Bot 59:24792497 Google Scholar
Cardinali, V C B, Dias, A C R, Mueller, T C, Abercrombie, L, Stewart, C N Jr., Tornisielo, V L, Christoffoleti, P J. (2015) Shikimate accumulation, glyphosate absorption and translocation in horseweed biotypes. Planta Daninha 33:109118 Google Scholar
Caseley, JC, Coupland, D (1985) Environmental and plant factors affecting glyphosate uptake movement and acidity. Pages 92123 in Grossbard E, Atkinson DA, eds. The Herbicide Glyphosate. London: Butterworths Google Scholar
Cassan-Wang, H, Soler, M, Yu, H, Camargo, El, Carocha, V, Ladouce, N, Savelli, B, Paiva, , Leplé, JC, Grima-Pettenati, J (2012) Reference genes for high-throughput quantitative reverse transcription–PCR analysis of gene expression in organs and tissues of Eucalyptus grown in various environmental conditions. Plant Cell Physiol 53:21012116 Google Scholar
Chiou, TJ, Lin, SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185206 Google Scholar
Coupland, D, Caseley, JC (1979) Presence of 14C activity in root exudates and guttation fluid from Agropyron repens treated with 14C-labelled glyphosate. New Phytol 83:1722 Google Scholar
Coupland, D, Peabody, DV (1981) Absorption, translocation, and exudation of glyphosate, fosamine, and amitrole in field horsetail (Equisetum arvense). Weed Sci 29:556560 Google Scholar
Daram, P, Brunner, S, Rausch, C, Steiner, C, Amrhein, N, Bucher, M (1999) Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell 11:21532166 Google Scholar
De Jonge, H, De Jonge, LW, Jacobsen, OH., Yamaguchi, T, Moldrup, P (2001) Glyphosate sorption in soils of different pH and phosphorus content. Soil Sci 166:230238 Google Scholar
Denis, MH, Delrot, S (1993) Carrier-mediate uptake of glyphosate in brad bean (Vicia faba) via a phosphate transporter. Physiol Plant 87:569575 Google Scholar
De Ruiter, H, Meinen, E (1996) Adjuvant-increased glyphosate uptake by protoplasts isolated from quackgrass Elytrigia repens (L.) Nevski. Weed Sci 44:3845 Google Scholar
De Ruiter, H, Verbeek, MAM, Uffing, AM (1988) Mode of action of a nonionic and a cationic surfactant in relation to glyphosate. Pages 4455 in Cross B, Scher HB, eds., Pesticide Formulations, Innovations and Developments. Washington, DC: American Chemical Society Google Scholar
Dewey, SA, Appleby, APA (1983) Comparison between glyphosate and assimilate translocation patterns in tall morning glory (Ipomoea purpurea). Weed Sci 31:308314 Google Scholar
Fitzgibbon, J, Braymer, HD (1988) Phosphate starvation induces uptake of glyphosate by Pseudomonas sp. strain PG2982. Appl Environ Microbiol 54:18861888 Google Scholar
Franz, JE, Mao, MK, Sikorski, JA (1997) Glyphosate: A Unique Global Herbicide. Washington, DC: American Chemical Society Google Scholar
Fiske, CH, Subbarow, Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:373400 Google Scholar
Gamuyao, R, Chin, JH, Pariasca-Tanaka, J, Pesaresi, P, Catausan, S, Dalid, C, Slamet-Loedin, I, Tecson-Mendoza, EM, Wissuwa, M, Heuer, S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488:535539 Google Scholar
Gomes, MP, Maccario, S, Lucotte, M, Labrecque, M, Juneau, P (2015) Consequences of phosphate application on glyphosate uptake by roots: impacts for environmental management practices. Sci Total Environ 276:97104 Google Scholar
Gottrup, O, O’Sullivan, PA, Shraa, RJ, Vanden, WH (1976) Uptake, translocation, metabolism and selectivity of glyphosate in Canada thistle and leafy spurge. Weed Res 16:197201 Google Scholar
Gougler, JA, Geiger, DR (1981) Uptake and distribution of N-(phosphonomethyl) glycine in sugar beet plants. Plant Physiol 68:668672 Google Scholar
Gu, M, Chen, A, Sun, S, Xu, G (2016) Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: what is missing? Mol Plant 9:396416 Google Scholar
Hamburger, D, Rezzonico, E, MacDonald-Comber Petétot, J, Somerville, C, Poirier, Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889902 Google Scholar
Hammond, JP, Bennett, MJ, Bowen, HC, Broadley, MR, Eastwood, DC, May, ST, Rahn, C, Swarup, R, Woolaway, KE, White, PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 13:578586 Google Scholar
Hoagland, DR, Arnon, DI. (1950) The Water Culture Method for Growing Plants without Soils. Berkeley: California Agricultural Experimental Station Google Scholar
Honegger, JL, Brooks, JM, Anderson, EJ, Porter, CA (1986) Glyphosate transport in plants. Pages 216268 in Cornshaw J, Lucas WJ, Giaquinta RT, eds. Phloem Transport. New York: Liss Google Scholar
Ibaoui, HE, Delrot, S, Besson, J, Bonnemain, JL (1986) Uptake and release of a non phloem-mobile (iprodione) xenobiotic by broadbean leaf tissues. Physiol Vég 24:431442 Google Scholar
Jachetta, JJ, Appleby, AP, Boersma, DL (1986) Apoplastic and symplastic pathways of atrazine and glyphosate transport in shoots of seedling sunflower. Plant Physiol 82:10001007 Google Scholar
Jain, A, Poling, MD, Karthikeyan, AS, Blakeslee, JJ, Peer, WA, Titapiwatanakun, B, Murphy, AS, Raghothama, KG (2007) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144:232247 Google Scholar
Karthikeyan, A, Varadarajan, D, Mukatira, U, Paino D’urzo, M, Damsz, B, Raghothama, K (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221233 Google Scholar
Kochian, LV (2012) Rooting for more phosphorus. Nature 488:466467 Google Scholar
Kretzmer, K, Hughes, M, Maines, L, Sammons, D. (2007) Assay comparison for measuring shikimate in glyphosate-treated plant species. 2007 North Central Weed Science Society Proceedings 62:36 Google Scholar
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ, Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:29472948 Google Scholar
Lee, RB (1993) Control of net uptake of nutrients by regulation of influx in barley plants recovering from nutrient deficiency. Ann Bot 72:223230 Google Scholar
Li, K, Xu, C, Li, Z, Zhang, K, Yang, A, Zhang, J (2008) Comparative proteome analyses of phosphorus response in maize (Zea mays L.) roots of wild-type and a low-P-tolerant mutant reveal root characteristics associated with phosphorus deficiency. Plant J 55:927939 Google Scholar
Li, K, Xu, C, Zhang, K, Yang, Y, Zhang, J (2007) Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants. Proteomics 7:15011512 Google Scholar
Lin, WD, Liao, YY, Yang, TJ, Pan, CY, Buckhout, TJ, Schmidt, W (2011) Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling. Plant Physiol 155:13831402 Google Scholar
Linsmaier, EM, Skoog, F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100127 Google Scholar
Liu, TY1, Huang, TK, Tseng, CY, Lai, YS, Lin, SI, Lin, WY, Chen, JW, Chiou, TJ (2012) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis . Plant Cell 24:21682183 Google Scholar
Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408<COMP: Please set (-Delta Delta C(T)) as superscript: −ΔΔCT.>>Google Scholar
Martin, RA, Edgington, LV (1981) Comparative systemic translocation of several xenobiotics and sucrose. Pestic Biochem Physiol 16:8796 Google Scholar
Misson, J, Raghothama, KG, Jain, A, Jouhet, J, Block, MA, Bligny, R, Ortet, P, Creff, A, Somerville, S, Rolland, N, Doumas, P, Nacry, P, Herrerra-Estrella, L, Nussaume, L, Thibaud, MC (2005) Genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:1193411939 Google Scholar
Mithila, J, Swanton, CJ, Blackshaw, RE, Cathcart, RJ, Hall, JC (2008) Physiological basis for reduced glyphosate efficacy on weeds grown under low soil nitrogen. Weed Sci 56:1217 Google Scholar
Monquero, PA, Christoffoleti, PJ, Osuna, MD, De Prado, RA ( 2004) Absorção, translocação e metabolismo do glyphosate por plantas tolerantes e suscetíveis a este herbicida. Planta Daninha 22:445451 Google Scholar
Morcuende, R, Bari, R, Gibon, Y, Zheng, W, Pant, BD, Bläsing, O, Usadel, B, Czechowski, T, Udvardi, MK, Stitt, M, Scheible, WR (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85112 Google Scholar
Morin, F, Vera, V, Nurit, F, Tissut, M, Marigo, G (1997) Glyphosate uptake in Catharanthus roseus cells: role of a phosphate transporter. Pestic Biochem Physiol 58:1322 Google Scholar
Muchhal, US, Pardo, JM, Raghothama, KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana . Proc Natl Acad Sci USA 93:1051910523 Google Scholar
Mudge, SR, Rae, AL, Diatloff, E, Smith, FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis . Plant J 31:341353 Google Scholar
Myburg, AA, Grattapaglia, D, Tuskan, GA, Hellsten, U, Hayes, RD, Grimwood, J, Jenkins, J, Lindquist, E, Tice, H, Bauer, D, Goodstein, DM, Dubchak, I, Poliakov, A, Mizrachi, E, Kullan, AR, Hussey, SG, Pinard, D, van der Merwe, K, Singh, P, van Jaarsveld, I, Silva-Junior, OB, Togawa, RC, Pappas, MR, Faria, DA, Sansaloni, CP, Petroli, CD, Yang, X, Ranjan, P, Tschaplinski, TJ, Ye, CY, Li, T, Sterck, L, Vanneste, K, Murat, F, Soler, M, Clemente, HS, Saidi, N, Cassan-Wang, H, Dunand, C, Hefer, CA, Bornberg-Bauer, E, Kersting, AR, Vining, K, Amarasinghe, V, Ranik, M, Naithani, S, Elser, J, Boyd, AE, Liston, A, Spatafora, JW, Dharmwardhana, P, Raja, R, Sullivan, C, Romanel, E, Alves-Ferreira, M, Külheim, C, Foley, W, Carocha, V, Paiva, J, Kudrna, D, Brommonschenkel, SH, Pasquali, G, Byrne, M, Rigault, P, Tibbits, J, Spokevicius, A, Jones, RC, Steane, DA, Vaillancourt, RE, Potts, BM, Joubert, F, Barry, K, Pappas, GJ, Strauss, SH, Jaiswal, P, Grima-Pettenati, J, Salse, J, Van de Peer, Y, Rokhsar, DS, Schmutz, J (2014) The genome of Eucalyptus grandis . Nature 510:356362 Google Scholar
[NCBI] National Center for Biotechnology Information Resource Coordinators (2017) Database resources of the NCBI. Nucleic Acids Res 45(D1): D12D17. https://doi.org10.1093/nar/gkw1071 Google Scholar
Neumann, G, Kohls, S, Landsberg, E, Stock-Oliveira Souza, K, Yamada, T, Römheld, V (2006) Relevance of glyphosate transfer to non-target plants via the rhizosphere. J Plant Dis Prot 20:963969 Google Scholar
Oliveira, LA, Breton, MC, Bastolla, FM, Camargo, RM, Frazzon, J, Pasquali, G (2012) Reference genes for the normalization of gene expression in Eucalyptus species. Plant Cell Physiol 53:405422 Google Scholar
Pipke, R, Amrhein, N (1988) Degradation of the phosphonate herbicide glyphosate by Arthrobacter utracyaneus ATCC 13752. Appl Environ Microbiol 54:12931296 Google Scholar
Pipke, R, Schulz, A, Amrhein, N (1987) Uptake of glyphosate by an Arthrobacter sp. Appl Environ Microbiol 53:974978 Google Scholar
Raghothama, KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665693 Google Scholar
Richard, EP, Slife, FW (1979) In vivo and in vitro characterization of the foliar entry of glyphosate in hemp dogbane (Apocynum cannabinum). Weed Sci 27:426433 Google Scholar
Rodrigues, JVJ, Worsham, AD, Corbin, FT (1982) Exudation of glyphosate from wheat (Triticum aestivum) plants and its effects on interplanted corn (Zea mays) and soybeans (Glycine max). Weed Sci 3:316320 Google Scholar
Rouached, H, Arpat, AB, Poirier, Y (2010) Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant 3:288299 Google Scholar
Rubio, V, Linhares, F, Solano, R, Martin, AC, Iglesias, J, Leyva, A, Paz-Ares, J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Gene Dev 15:21222133 Google Scholar
Saitou, N, Nei, M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406425 Google Scholar
Satichivi, NM, Wax, LM, Stoller, EW, Briskin, DP (2000) Absorption and translocation of glyphosate isopropylamine and trimethysulfonium salts in Abutilon theophrasti and Setaria faberi . Weed Sci 48:675679 Google Scholar
Schultz, ME, Amrhein, N (1984) Glyphosate induced accumulation of shikimic acid in tomato plants in relation to the translocation of glyphosate. Plant Physiol 7:3749 Google Scholar
Schultz, ME, Burnside, OC (1980) Absorption, translocation, and metabolism of 2,4-D and glyphosate in hemp dogbane (Apocynum cannabinum). Weed Sci 2:1320 Google Scholar
Secco, D, Baumann, A, Poirier, Y (2010) Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiol 52:16931704 Google Scholar
Shaner, DL, Nadler‐Hassar, T, Henry, WB, Koger, CH (2005) A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci 53:769774 Google Scholar
Sherrick, SL, Holt, HA Hess, FD (1986) Absorption and translocation of MON 0818 adjuvant in field bindweed (Convolvulus arvensis). Weed Sci 34:817823 Google Scholar
Shinabarger, DL, Braymer, HD (1986) Glyphosate catabolism by Pseudomonas sp. strain PG2982. J Bacteriol 168:702707 Google Scholar
Sprankle, P, Meggitt, WF, Penner, D (1975) Adsorption, mobility, and microbial degradation of glyphosate in the soil. Weed Sci 23:229234 Google Scholar
Sun, S, Gu, M, Cao, Y, Huang, X, Zhang, X, Ai, P, Zhao, J, Fan, X, Xu, G (2012) A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiol 159:15711581 Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A, Kumar, S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:27252729 Google Scholar
[TAIR] The Arabidopsis Information Resource (2017) aboutarabidopsis.html, on www.arabidopsis.org. Accessed: July 31, 2017Google Scholar
Tesfamariam, T, Bott, S, Cakmak, I, Römheld, V, Neumann, G (2009) Glyphosate in the rhizosphere-role of waiting times and different glyphosate binding forms in soils for phytotoxicity to non-target plants. Eur J Agron 31:126132 Google Scholar
Tilquin, M, Peltier, JP, Marigo, G (2000) Mechanisms for the coupling of iron and glyphosate uptake in Catharanthus roseus cells. Pestic Biochem Physiol 67:145154 Google Scholar
Versaw, WK, Harrison, MH (2002) A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14:17511766 Google Scholar
Wang, Y, Ribot, C, Rezzonico, E, Poirier, Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol 135:400411 Google Scholar
Wang, Y, Secco, D, Poirier, Y (2008) Characterization of the PHO1 gene family and the responses to phosphate deficiency of Physcomitrella patens . Plant Physiol 146:646656 Google Scholar
Wu, P, Ma, L, Hou, X, Wang, M, Wu, Y, Liu, F, Deng, XW (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:12601271 Google Scholar
Wyrill, JB, Burnside, OC (1976) Absorption, translocation and metabolism of 2,4-D and glyphosate in common milkweed and hemp dogbane. Weed Sci 24:557566 Google Scholar
Xu, J, Li, G, Wang, Z, Si, L, He, S, Cai, J, Huang, J, Donovan, MD (2016) The role of L-type amino acid transporters in the uptake of glyphosate across mammalian epithelial tissues. Chemosphere 145:487494 Google Scholar
Zablotowicz, RM, Reddy, KN (2007) Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Protect 26:370376 Google Scholar