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Plant function and evolutionary biology
RESEARCH ARTICLE

PvUPS1 plays a role in source–sink transport of allantoin in French bean (Phaseolus vulgaris)

Hélène C. Pélissier A and Mechthild Tegeder A B
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Center for Integrated Biotechnology, Center for Reproductive Biology, Washington State University, Pullman, WA 99164, USA.

B Corresponding author. Email: tegeder@wsu.edu

C This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.

Functional Plant Biology 34(4) 282-291 https://doi.org/10.1071/FP06277
Submitted: 27 October 2006  Accepted: 6 December 2006   Published: 19 April 2007

Abstract

Nodulated tropical legumes such as French bean (Phaseolus vulgaris L.) receive their nitrogen via N-fixing rhizobia. The principal products of fixed nitrogen are the ureides allantoin and allantoic acid that are synthesised in root nodules and then translocated to the mature leaves of the shoot via the xylem. By feeding [14C]allantoin to mature leaves and roots of French bean plants we showed that this ureide is transported over long distances by xylem and then phloem to developing organs such as pods, root tips and growing leaves. For analysis of allantoin partitioning within the plant, concentrations of allantoin in French bean organs and xylem sap were determined. The amounts of allantoin varied between organs, with the highest levels being detected in the stems. Differences in levels of allantoin were found between nodulated and non-nodulated plants, with generally higher allantoin concentrations in tissues and xylem sap of nodulated plants. RNA and protein expression of the recently identified French bean allantoin permease PvUPS1 (AY461734) was detected in all plant organs indicating a function in allantoin transport throughout the plant. The levels of PvUPS1 expression were consistent with the allantoin concentrations in the different organs. In situ RNA hybridisation studies were carried out and showed that PvUPS1 is expressed in the phloem throughout the plant. Together, our results indicate that in French bean allantoin is transported from source to sink and that PvUPS1 plays a role in phloem loading and in allantoin transport to developing sinks.

Additional keywords: nitrogen partitioning, ureide transport.


Acknowledgements

We acknowledge the late Vince Franceschi for all his help with the microscopy and identification of anatomical features. The assistance of Valerie Lynch Holmes and Chris Davitt at the WSU Franceschi Microscopy and Imaging Center is appreciated. We thank Nathan Tarlyn for his technical assistance and Chuck Cody for his help in the greenhouse. We also acknowledge the financial support by grant 2001–35318–10990 from the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service and by grant IOB 0448506 from the National Science Foundation.


References


Atkins C , Beevers L (1990) Synthesis, transport and utilization of translocated solutes of nitrogen. In ‘Nitrogen in higher plants’. (Ed. YP Abrol) pp. 233–295. (Research Studies Press: Somerset, UK)

Atkins CA, Pate JS, Ritchie A, Peoples MB (1982) Metabolism and translocation of allantoin in ureide-producing grain legumes. Plant Physiology 70, 476–482.
PubMed |
open url image1

Becher M, Schepl U, Schubert S (1997) N2 fixation during different physiological stages of Phaseolus vulgaris OAC Rico and its supernodulating mutant R32BS15: the role of assimilate supply to and export from nodules. Journal of Plant Physiology 150, 31–36. open url image1

Benedito VA, Dai XB, He J, Zhao PX, Udvardi MK (2006) Functional genomics of plant transporters in legume nodules. Functional Plant Biology 33, 731–736.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Crews TE, Brockwell J, Peoples MB (2004) Host-rhizobia interaction for effective inoculation: evaluation of the potential use of the ureide assay to monitor the symbiotic performance of tepary bean (Phaseolus acutifolius A.Gray). Soil Biology and Biochemistry 36, 1223–1228.
Crossref | GoogleScholarGoogle Scholar | open url image1

Franceschi VR, Tarlyn NM (2002) L-ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiology 130, 649–656.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hansen AP, Rerkasem B, Lordkaew S (1995) Does ammonium uptake influence xylem sap composition in Phaseolus vulgaris L. and Glycine max (L.) Merill. Experientia 51, 1085–1089.
Crossref | GoogleScholarGoogle Scholar | open url image1

Herridge DF (1982) Relative abundance of ureides and nitrate in plant tissues of soybean as a quantitative assay of nitrogen fixation. Plant Physiology 70, 1–6.
PubMed |
open url image1

Herridge DF, Atkins CA, Pate JS, Rainbird RM (1978) Allantoin and allantoic acid in the nitrogen economy of the cowpea [Vigna unguiculata (L.) Walp.]. Plant Physiology 62, 495–498.
PubMed |
open url image1

Hsu FC, Bennett AB, Spanswick RM (1984) Concentrations of sucrose and nitrogenous compounds in the apoplast of developing soybean seed coats and embryos. Plant Physiology 75, 181–186.
PubMed |
open url image1

Keates SE, Tarlyn NM, Loewus FA, Franceschi VR (2000) l-Ascorbic acid and l-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes. Phytochemistry 53, 433–440.
Crossref | l
-Ascorbic acid and l-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes.&journal=Phytochemistry&volume=53&pages=433-440&publication_year=2000&author=VR%20Franceschi&hl=en&doi=10.1016/S0031-9422(99)00448-3" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed | open url image1

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant, Cell & Environment 26, 37–56.
Crossref | GoogleScholarGoogle Scholar | open url image1

Layzell DB, LaRue TA (1982) Modeling C and N transport to developing soybean fruits. Plant Physiology 70, 1290–1298.
PubMed |
open url image1

Matsumoto T, Yatazawa M, Yamamoto Y (1977a) Distribution and change in the contents of allantoin and allantoic acid in developing nodulating and non-nodulating soybean plants. Plant and Cell Physiology 18, 353–359. open url image1

Matsumoto T, Yatazawa M, Yamamoto Y (1977b) Effects of exogenous nitrogenous-compounds on the concentrations of allantoin and various constituents in several organs of soybean plants. Plant and Cell Physiology 18, 613–624. open url image1

McClure PR, Israel DW (1979) Transport of nitrogen in the xylem of soybean plants. Plant Physiology 64, 411–416.
PubMed |
open url image1

Mothes K (1961) The metabolism of urea and ureides. Canadian Journal of Botany 39, 1785–1807. open url image1

Pate JS, Sharkey PJ, Lewis OAM (1975) Xylem to phloem transfer of solutes in fruiting shoots of legumes, studied by a phloem bleeding technique. Planta 122, 11–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pate JS, Atkins CA, White ST, Rainbird RM, Woo KC (1980) Nitrogen nutrition and xylem transport of nitrogen in ureide-producing grain legumes. Plant Physiology 65, 961–965.
PubMed |
open url image1

Pate JS, Peoples MB, Atkins CA (1984) Spontaneous phloem bleeding from cryopunctured fruits of a ureide producing legume. Plant Physiology 74, 499–505.
PubMed |
open url image1

Pélissier HC, Frerich A, Desimone M, Schumacher K, Tegeder M (2004) PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiology 134, 664–675.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Penacabriales JJ, Gragedacabrera OA, Kola V, Hardarson G (1993) Time-course of N2 fixation in common bean (Phaseolus vulgaris L.). Plant and Soil 152, 115–121.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rainbird RM, Thorne JH, Hardy RWF (1984) Role of amides, amino acids, and ureides in the nutrition of developing soybean seeds. Plant Physiology 74, 329–334.
PubMed |
open url image1

Schubert KR (1986) Products of biological nitrogen fixation in higher plants: synthesis, transport and metabolism. Annual Review of Plant Physiology 37, 539–574.
Crossref | GoogleScholarGoogle Scholar | open url image1

Smith PMC, Atkins CA (2002) Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiology 128, 793–802.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Streeter JG (1979) Allantoin and allantoic acid in tissues and stem exudate from field-grown soybean plants. Plant Physiology 63, 478–480.
PubMed |
open url image1

Streeter JG (2005) Effects of nitrogen and calcium supply on the accumulation of oxalate in soybean seeds. Crop Science 45, 1464–1468.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thomas RJ, Feller U, Erismann KH (1979) The effect of different inorganic nitrogen sources and plant age on the composition of bleeding sap of Phaseolus vulgaris. New Phytologist 82, 657–669.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thomas RJ, Feller U, Erismann KH (1980) Ureide metabolism in non-nodulated Phaseolus vulgaris L. Journal of Experimental Botany 31, 409–417.
Crossref |
open url image1

Thomas RJ, Schrader LE (1981) Ureide metabolism in higher plants. Phytochemistry 20, 361–371.
Crossref | GoogleScholarGoogle Scholar | open url image1

Todd CD, Tipton PA, Blevins DG, Piedras P, Pineda M, Polacco JC (2006) Update on ureide degradation in legumes. Journal of Experimental Botany 57, 5–12.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1