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Auxin as Long-Distance Signal Controlling Root Architecture in Response to Nitrogen

  • Giel E. van Noorden
  • Ulrike Mathesius
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 19)

Abstract

Plants show extensive root plasticity in response to nitrogen availability. Lateral root initiation and emergence are affected by nitrogen concentration and distribution to coordinate the ability to capture maximum nitrogen while minimizing carbon expenditure. Legumes and actinorhizal plants have additionally evolved symbioses with nitrogen-fixing bacteria that leads to the formation of nodules. Nodule numbers are controlled by systemic autoregulation of nodulation (AON) signaling through a receptor-like kinase acting in the shoot. The AON genes also control lateral root formation in response to nitrogen to varying extents in different legumes. Auxin transport control from the shoot to the root is one of the signals affecting nodule and lateral root development, and this is under the control of the AON gene in the legume Medicago truncatula. Nitrogen availability modulates long-distance auxin transport and this partly requires the function of the AON gene. Thus we propose a model in which nitrogen availability is perceived in the shoot, is processed by the AON gene, and feeds back on root architecture via control of shoot-to-root auxin transport.

Keywords

Auxin transport Nitrogen Root development Nodulation Autoregulation 

Notes

Acknowledgements

We thank the Australian Research Council for funding through an ARC discovery grant (DP120102970) and a Future Fellowship to UM (FT100100669).

References

  1. Alvarez JM, Vidal EA, Gutierrez RA (2012) Integration of local and systemic signaling pathways for plant N responses. Curr Opin Plant Biol 15:185–191PubMedCrossRefGoogle Scholar
  2. Bao J, Chen F, Gu R, Wang G, Zhang F, Mi G (2007) Lateral root development of two Arabidopsis auxin transport mutants, auxl-7 and eirl-1, in response to nitrate supplies. Plant Sci 173:417–425CrossRefGoogle Scholar
  3. Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29:325–332PubMedCrossRefGoogle Scholar
  4. Boot KJM, van Brussel AAN, Tak T, Spaink HP, Kijne JW (1999) Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp nigra roots. Mol Plant-Microbe Interact 12:839–844CrossRefGoogle Scholar
  5. Caba JM, Recalde L, Ligero F (1998) Nitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa. Plant Cell Environ 21:87–93CrossRefGoogle Scholar
  6. Caba JM, Centeno ML, Fernandez B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211:98–104PubMedCrossRefGoogle Scholar
  7. Carroll BJ, McNeil DL, Gresshoff PM (1985a) Isolation and properties of soybean Glycine max (L) Merr mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci USA 82:4162–4166PubMedCrossRefGoogle Scholar
  8. Carroll BJ, McNeil DL, Gresshoff PM (1985b) A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol 78:34–40PubMedCrossRefGoogle Scholar
  9. Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inze D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852PubMedGoogle Scholar
  10. Day DA, Caroll BJ, Delves AC, Gresshoff PM (1989) Relationship between autoregulation and nitrate inhibition in soybeans. Physiol Plant 75:37–42CrossRefGoogle Scholar
  11. Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gresshoff PM (1986) Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82:588–590PubMedCrossRefGoogle Scholar
  12. Dubrovsky JG, Napsucialy-Mendivil S, Duclercq J, Cheng Y, Shishkova S, Ivanchenko MG, Friml J, Murphy AS, Benkovà E (2011) Auxin minimum defines a developmental window for lateral root initiation. New Phytol 191:970–983PubMedCrossRefGoogle Scholar
  13. Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224PubMedCrossRefGoogle Scholar
  14. Friml J (2003) Auxin transport – shaping the plant. Curr Opin Plant Biol 6:7–12PubMedCrossRefGoogle Scholar
  15. Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256:111–137PubMedCrossRefGoogle Scholar
  16. Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283PubMedCrossRefGoogle Scholar
  17. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808PubMedCrossRefGoogle Scholar
  18. Guo YF, Chen FJ, Zhang FS, Mi GH (2005) Auxin transport from shoot to root is involved in the response of lateral root growth to localized supply of nitrate in maize. Plant Sci 169:894–900CrossRefGoogle Scholar
  19. Gutierrez RA, Lejay LV, Dean A, Chiaromonte F, Shasha DE, Coruzzi GM (2007) Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8:R7PubMedCrossRefGoogle Scholar
  20. Hayashi S, et al 2013 Systemic signalling in legume nodulation: nodule formation and its regulation. In: Baluska F (ed) Long-distance systemic signaling and communication in plants. Springer, Heidelberg.Google Scholar
  21. Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86:1244–1248PubMedCrossRefGoogle Scholar
  22. Jeudy C, Ruffel S, Freixes S, Tillard P, Santoni AL, Morel S, Journet E-P, Duc G, Gojon A, Lepetit M, Salon C (2010) Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses. New Phytol 185:817–828PubMedCrossRefGoogle Scholar
  23. Jin J, Watt M, Mathesius U (2012) The autoregulation gene SUNN mediates changes in root organ formation in response to nitrogen through alteration of shoot-to-root auxin transport. Plant Physiol 159:489–500PubMedCrossRefGoogle Scholar
  24. Kosslak RM, Bohlool BB (1984) Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiol 75:125–130PubMedCrossRefGoogle Scholar
  25. Krouk G, Crawford NM, Coruzzi GM, Tsay Y-F (2010a) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:266–273PubMedCrossRefGoogle Scholar
  26. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010b) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937PubMedCrossRefGoogle Scholar
  27. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426PubMedCrossRefGoogle Scholar
  28. Kuppusamy KT, Ivashuta S, Bucciarelli B, Vance CP, Gantt JS, VandenBosch KA (2009) Knockdown of CELL DIVISION CYCLE16 reveals an inverse relationship between lateral root and nodule numbers and a link to auxin in Medicago truncatula. Plant Physiol 151:1155–1166PubMedCrossRefGoogle Scholar
  29. Linkohr BI, Williamson LC, Fitter AH, Leyser HMO (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760PubMedCrossRefGoogle Scholar
  30. Liu J, An X, Cheng L, Chen F, Bao J, Yuan L, Zhang F, Mi G (2010) Auxin transport in maize roots in response to localized nitrate supply. Ann Bot 106:1019–1026PubMedCrossRefGoogle Scholar
  31. Malamy JE, Ryan KS (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol 127:899–909PubMedCrossRefGoogle Scholar
  32. Marchant A, Bhalerao R, Casimiro I, Eklof J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597PubMedCrossRefGoogle Scholar
  33. Mathesius U (2008) Auxin: at the root of nodule development? Funct Plant Biol 35:651–668CrossRefGoogle Scholar
  34. Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34PubMedCrossRefGoogle Scholar
  35. Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D’Haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153:222–237PubMedCrossRefGoogle Scholar
  36. Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S (2012) Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J 70:367–376PubMedCrossRefGoogle Scholar
  37. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429PubMedCrossRefGoogle Scholar
  38. Novak K, Lisa L, Skrdleta V (2011) Pleiotropy of pea RisfixC supernodulation mutation is symbiosis-independent. Plant Soil 342:173–182CrossRefGoogle Scholar
  39. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50:67–77PubMedCrossRefGoogle Scholar
  40. Pacios-Bras C, Schlaman HRM, Boot K, Admiraal P, Langerak JM, Stougaard J, Spaink HP (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Mol Biol 52:1169–1180PubMedCrossRefGoogle Scholar
  41. Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275:527–530PubMedCrossRefGoogle Scholar
  42. Penmetsa RV, Frugoli JA, Smith LS, Long SR, Cook DR (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol 131:998–1008PubMedCrossRefGoogle Scholar
  43. Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, Conejero G, Peret B, King JR, Verdeil JL, Hocher V, Franche C, Bennett MJ, Tisa LS, Laplaze L (2010) Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules. Plant Physiol 154:1372–1380PubMedCrossRefGoogle Scholar
  44. Prayitno J, Rolfe BG, Mathesius U (2006) The ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiol 142:168–180PubMedCrossRefGoogle Scholar
  45. Reed RC, Brady SR, Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol 118:1369–1378PubMedCrossRefGoogle Scholar
  46. Reid DE, Ferguson BJ, Gresshoff PM (2011a) Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant-Microbe Interact 24:606–618PubMedCrossRefGoogle Scholar
  47. Reid DE, Ferguson BJ, Hayashi S, Lin Y-H, Gresshoff PM (2011b) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108:789–795PubMedCrossRefGoogle Scholar
  48. Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339CrossRefGoogle Scholar
  49. Rightmyer AP, Long SR (2011) Pseudonodule formation by wild-type and symbiotic mutant Medicago truncatula in response to auxin transport inhibitors. Mol Plant-Microbe Interact 24:1372–1384PubMedCrossRefGoogle Scholar
  50. Ruffel S, Krouk G, Ristova D, Shashka D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci USA 108:18514–18529CrossRefGoogle Scholar
  51. Sagan M, Morandi D, Tarenghi E, Duc G (1995) Selection of nodulation and mycorrhizal mutants in the model-plant Medicago truncatula (Gaertn) after gamma-ray mutagenesis. Plant Sci 111:63–71CrossRefGoogle Scholar
  52. Salon C, Lepetit M, Gamas P, Jeudy C, Moreau S, Moreau D, Voisin A-S, Duc G, Bourion V, Munier-Jolain N (2009) Analysis and modeling of the integrative response of Medicago truncatula to nitrogen constraints. C R Biol 332:1022–1033PubMedCrossRefGoogle Scholar
  53. Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58:809–822PubMedCrossRefGoogle Scholar
  54. Schnabel E, Mukherjee A, Smith L, Kassaw T, Long S, Frugoli J (2010) The lss supernodulation mutant of Medicago truncatula reduces expression of the SUNN Gene. Plant Physiol 154:1390–1402PubMedCrossRefGoogle Scholar
  55. Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112PubMedCrossRefGoogle Scholar
  56. Streeter J (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23CrossRefGoogle Scholar
  57. Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139:3997–4006PubMedCrossRefGoogle Scholar
  58. Takanashi K, Sugiyama A, Yazaki K (2011) Involvement of auxin distribution in root nodule development of Lotus japonicus. Planta 234:73–81PubMedCrossRefGoogle Scholar
  59. Tamaki V, Mercier H (2007) Cytokinins and auxin communicate nitrogen availability as long-distance signal molecules in pineapple (Ananas comosus). J Plant Physiol 164:1543–1547PubMedCrossRefGoogle Scholar
  60. Tian Q, Chen F, Liu J, Zhang F, Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J Plant Physiol 165:942–951PubMedCrossRefGoogle Scholar
  61. van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol 140:1494–1506PubMedCrossRefGoogle Scholar
  62. van Noorden GE, Kerim T, Goffard N, Wiblin R, Pellerone FI, Rolfe BG, Mathesius U (2007) Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol 144:1115–1131PubMedCrossRefGoogle Scholar
  63. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutierrez RA (2010) Nitrate-responsive miRNA393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:4477–4482PubMedCrossRefGoogle Scholar
  64. Walch-Liu P, Filleur S, Gan YB, Forde BG (2005) Signaling mechanisms integrating root and shoot responses to changes in the nitrogen supply. Photosynth Res 83:239–250PubMedCrossRefGoogle Scholar
  65. Walch-Liu P, Ivanov II, Filleur S, Gan YB, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot 97:875–881PubMedCrossRefGoogle Scholar
  66. White J, Prell J, James EK, Poole P (2007) Nutrient sharing between symbionts. Plant Physiol 144:604–614PubMedCrossRefGoogle Scholar
  67. Wightman F, Schneider EA, Thimann KV (1980) Hormonal factors controlling the initiation and development of lateral roots. II. Effects of exogenous growth factors on lateral root formation in pea roots. Physiol Plant 49:304–314CrossRefGoogle Scholar
  68. Wopereis J, Pajuelo E, Dazzo FB, Jiang QY, Gresshoff PM, de Bruijn FJ, Stougaard J, Szczyglowski K (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23:97–114PubMedCrossRefGoogle Scholar
  69. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409PubMedCrossRefGoogle Scholar
  70. Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Plant Science Division, Research School of BiologyAustralian National UniversityCanberraAustralia

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