Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Functional genomics of plant transporters in legume nodules

Vagner A. Benedito A , Xinbin Dai A , Ji He A , Patrick X. Zhao A and Michael K. Udvardi A B C
+ Author Affiliations
- Author Affiliations

A Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK 73401, USA.

B Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Golm, Germany.

C Corresponding author. Email: mudvardi@noble.org

D This paper originates from a presentation at the Third International Conference on Legume Genomics and Genetics, Brisbane, Queensland, Australia, April 2006.

Functional Plant Biology 33(8) 731-736 https://doi.org/10.1071/FP06085
Submitted: 11 April 2006  Accepted: 25 May 2006   Published: 2 August 2006

Abstract

Over the past few decades, a combination of physiology, biochemistry, molecular and cell biology, and genetics has given us a basic understanding of some of the key transport processes at work in nitrogen-fixing legume nodules, especially those involved in nutrient exchange between infected plant cells and their endosymbiotic rhizobia. However, our knowledge in this area remains patchy and dispersed over numerous legume species. Recent progress in the areas of genomics and functional genomics of the two model legumes, Medicago truncatula and Lotus japonicus is rapidly filling the gap in knowledge about which plant transporter genes are expressed constitutively in nodules and other organs, and which are induced or expressed specifically in nodules. The latter class in particular is the focus of current efforts to understand specialised, nodule-specific roles of transporters. This article briefly reviews past work on the biochemistry and molecular biology of plant transporters in nodules, before describing recent work in the areas of transcriptomics and bioinformatics. Finally, we consider where functional genomics together with more classical approaches are likely to lead us in this area of research in the future.

Keywords: functional genomics, legume nodule, symbiotic nitrogen fixation, transporter.


Acknowledgments

We thank the Samuel Roberts Noble Foundation and the Max Planck Society for generous support of research in our laboratories, and the German DFG for specific funding related to legume nodule transport.


References


Andreev IM, Dubrovo PN, Krylova VV, Izmailov SF (1998) Calcium uptake by symbiosomes and the peribacteroid membrane vesicles isolated from yellow lupin root nodules. Journal of Plant Physiology 153, 610–614. open url image1

Andreev IM, Dubrovo PN, Krylova VV, Izmailov SF (1999) Functional identification of ATP-driven Ca2+ pump in the peribacteroid membrane of broad bean root nodules. FEBS Letters 447, 49–52.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Andreev I, Krylova V, Dubrovo P, Izmailov S (2005) Passive potassium transport by symbiosomes from broad bean root nodules. Plant Science 168, 1005–1010.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. The Plant Journal 39, 487–512.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiology 133, 462–469.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

D’Apuzzo E, Rogato A, Simon-Rosin U, El Alaoui H, Barbulova A , et al. (2004) Characterization of three functional high-affinity ammonium transporters in Lotus japonicus with differential transcriptional regulation and spatial expression. Plant Physiology 134, 1763–1774.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Desbrosses G, Kopka C, Ott T, Udvardi MK (2004) Lotus japonicus LjKUP is induced late during nodule development and encodes a potassium transporter of the plasma membrane. Molecular Plant–Microbe Interactions 17, 789–797.
PubMed |
open url image1

Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song KM, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. The Plant Journal 45, 616–629.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

El Yahyaoui F, Küster H, Ben Amor B, Hohnjec N, Puhler A , et al. (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiology 136, 3159–3176.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fedorova E, Thomson R, Whitehead LF, Maudoux O, Udvardi MK, Day DA (1999) Localization of H+-ATPases in root nodules. Planta 209, 25–32.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fedorova M, Mortel JVD, Matsumoto PA, Cho J, Town CD, VandenBosch KA, Gantt JS, Vance CP (2002) Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiology 130, 519–537.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Flemetakis EDM, Cotzur D, Efrose RC, Aivalakis G, Colebatch G, Udvardi M, Katinakis P (2003) A sucrose transporter, LjSUT4, is up-regulated during Lotus japonicus nodule development. Journal of Experimental Botany 54, 1789–1791.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hofmann K, Stoffel W (1993) Tmbase — a database of membrane spanning proteins segments. Biological Chemistry Hoppe-Seyler 347, 166. open url image1

Jeong J, Suh S, Guan C, Tsay YF, Moran N, Oh CJ, An CS, Demchenko KN, Pawlowski K, Lee Y (2004) A nodule-specific dicarboxylate transporter from alder is a member of the peptide transporter family. Plant Physiology 134, 969–978.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kaiser BN, Moreau S, Castelli J, Thomson R, Lambert A, Bogliolo S, Puppo A, Day DA (2003) The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. The Plant Journal 35, 295–304.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kouchi H, Shimomura K, Hata S, Hirota A, Wu GJ , et al. (2004) Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus. DNA Research 11, 263–274.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Krusell L, Krause K, Ott T, Desbrosses G, Kramer U , et al. (2005) The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. The Plant Cell 17, 1625–1636.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Küster H, Hohnjec N, Krajinski F, El YF, Manthey K , et al. (2004) Construction and validation of cDNA-based Mt6k-RIT macro- and microarrays to explore root endosymbioses in the model legume Medicago truncatula. Journal of Biotechnology 108, 95–113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

LeVier K, Day DA, Guerinot ML (1996) Iron uptake by symbiosomes from soybean root nodules. Plant Physiology 111, 893–900.
PubMed |
open url image1

López-Millán A-F, Ellis DR, Grusak MA (2004) Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Molecular Biology 54, 583–596.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Puhler A, Perlick AM, Kuster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Molecular Plant–Microbe Interactions 17, 1063–1077.
PubMed |
open url image1

Moreau S, Meyer JM, Puppo A (1995) Uptake of iron by symbiosomes and bacteroids from soybean nodules. FEBS Letters 361, 225–228.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Moreau S, Day DA, Puppo A (1998) Ferrous iron is transported across the peribacteroid membrane of soybean nodules. Planta 207, 83–87.
Crossref | GoogleScholarGoogle Scholar | open url image1

Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. Journal of Biological Chemistry 277, 4738–4746.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niemietz CM, Tyerman SD (2000) Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Letters 465, 110–114.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Obermeyer G, Tyerman SD (2005) NH4 + currents across the peribacteroid membrane of soybean. Macroscopic and microscopic properties, inhibition by Mg2+, and temperature dependence indicate a subpicoSiemens channel finely regulated by divalent cations. Plant Physiology 139, 1015–1029.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oldroyd GED, Harrison MJ, Udvardi M (2005) Peace talks and trade deals. Keys to long-term harmony in legume–microbe symbioses. Plant Physiology 137, 1205–1210.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Peiter E, Schubert S (2003) Sugar uptake and proton release by protoplasts from the infected zone of Vicia faba L. nodules: evidence against apoplastic sugar supply of infected cells. Journal of Experimental Botany 54, 1691–1700.
Crossref | GoogleScholarGoogle Scholar | 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

Roberts DM, Tyerman SD (2002) Voltage-dependent cation channels permeable to NH4 +, K+, and Ca2+ in the symbiosome membrane of the model legume Lotus japonicus. Plant Physiology 128, 370–378.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ronson CW, Lyttleton P, Robertson JG (1981) C4-dicarboxylate transport mutants of Rhizobium trifoli form ineffective nodules on Trifolium repens. Proceedings of the National Academy of Sciences USA 78, 4284–4288.
Crossref |
open url image1

Rosendahl L , Glenn AR , Dilworth MJ (1991) Organic and inorganic inputs into legume root nodule nitrogen fixation. In ‘Biology and biochemistry of nitrogen fixation.’ (Ed. AR Glenn) pp. 259–291.

Simon-Rosin U, Wood C, Udvardi MK (2003) Molecular and cellular characterisation of LjAMT2;1, an ammonium transporter from the model legume Lotus japonicus. Plant Molecular Biology 51, 99–108.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smil V (1999) Nitrogen in crop production: an account of global flows. Global Biogeochemical Cycles 13, 647–662.
Crossref | GoogleScholarGoogle Scholar | open url image1

Suganuma NYA, Itou A, Hakoyama T, Banba M, Hata S, Kawaguchi M, Kouchi H (2004) cDNA macroarray analysis of gene expression in ineffective nodules induced on the Lotus japonicus sen1 mutant. Molecular Plant–Microbe Interactions 17, 1223–1233.
PubMed |
open url image1

Tadege M, Ratet P, Mysore KS (2005) Insertional mutagenesis: a Swiss Army knife for functional genomics of Medicago truncatula. Trends in Plant Science 10, 229–235.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849–850.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tyerman SD, Whitehead LF, Day DA (1995) A channel-like transporter for NH4 + on the symbiotic interface of N2-fixing plants. Nature 378, 629–632.
Crossref | GoogleScholarGoogle Scholar | open url image1

Udvardi MK, Day DA (1989) Electrogenic ATPase activity on the peribacteroid membrane of soybean (Glycine max L.) root nodules. Plant Physiology 90, 982–987.
PubMed |
open url image1

Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annual Review of Plant Physiology and Plant Molecular Biology 48, 493–523.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Udvardi MK, Lister DL, Day DA (1991) ATPase activity and anion transport across the peribacteroid membrane of isolated soybean symbiosomes. Archives of Microbiology 156, 362–366.
Crossref | GoogleScholarGoogle Scholar | open url image1

Udvardi MK, Price GD, Gresshoff PM, Day DA (1988) A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Letters 231, 36–40.
Crossref | GoogleScholarGoogle Scholar | open url image1

Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends in Plant Science 10, 222–228.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vincill ED, Szczyglowski K, Roberts DM (2005) GmN70 and LjN70. Anion transporters of the symbiosome membrane of nodules with a transport preference for nitrate. Plant Physiology 137, 1435–1444.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wandrey M, Trevaskis B, Brewin N, Udvardi MK (2004) Molecular and cell biology of a family of voltage-dependent anion channel porins in Lotus japonicus. Plant Physiology 134, 182–193.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wienkoop S, Saalbach G (2003) Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiology 131, 1080–1090.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Young ND, Cannon SB, Sato S, Kim D, Cook DR, Town CD, Roe BA, Tabata S (2005) Sequencing the gene spaces of Medicago truncatula and Lotus japonicus. Plant Physiology 137, 1174–1181.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1