Auxin and Strigolactone Signaling are Required for Modulation of Arabidopsis Shoot Branching by Nitrogen Supply

Plant Physiology

Volumn 166, Issue 1, 2014, Pages 384-395

  Jong, Maaike De ^a   Ongaro, Veronica ^b   Ljung, Karin ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEACETIC ACID DERIVATIVE; LACTONE; NITRIC ACID DERIVATIVE; NITROGEN;

ARABIDOPSIS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SHOOT;

ARABIDOPSIS; INDOLEACETIC ACIDS; LACTONES; NITRATES; NITROGEN; PLANT SHOOTS;

EID: 84907055566     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.242388     Document Type: Article

References (90)

1. Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19: 458–472.
2. Balla J, Kalousek P, Reinöhl V, Friml J, Procházka S (2011) Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant J 65: 571–577.
3. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591–602.
4. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16: 553–563.
5. Beveridge CA, Ross JJ, Murfet IC (1996) Branching in pea (action of genes Rms3 and Rms4). Plant Physiol 110: 859–865.
6. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14: 1232–1238.
7. Booker J, Chatfield S, Leyser O (2003) Auxin acts in xylem-associated or medullary cells to mediate apical dominance. Plant Cell 15: 495–507.
8. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8: 443–449.
9. Bouguyon E, Gojon A, Nacry P (2012) Nitrate sensing and signaling in plants. Semin Cell Dev Biol 23: 648–654.
10. Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150: 482–493.
11. Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6: 18–28.
12. Brown BT, Foster C, Phillips JN, Rattigan BM (1979) The indirect role of 2,4-D in the maintenance of apical dominance in decapitated sunflower seedlings (Helianthus annuus L.). Planta 146: 475–480.
13. Carroll BJ, McNeil DL, Gresshoff PM (1985) A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol 78: 34–40.
14. Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6: 71–80.
15. Chen JG, Cheng SH, Cao W, Zhou X (1998) Involvement of endogenous plant hormones in the effect of mixed nitrogen source on growth and tillering of wheat. J Plant Nutr 21: 87–97.
16. Cline MG (1991) Apical dominance. Bot Rev 57: 318–358.
17. Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7: 859–868.
18. Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Müller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905–2913.
19. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386: 485–488.
20. Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12: 211–221.
21. Drew MC (1975) Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75: 479–490.
22. Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 14: 364–372.
23. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158: 487–498.
24. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2013) Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Mol Plant 6: 128–140.
25. Everat-Bourbouloux A, Bonnemain JL (1980) Distribution of labelled auxin and derivatives in stem tissues of intact and decapitated broad-bean plants in relation to apical dominance. Physiol Plant 50: 145–152.
26. Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17: 464–474.
27. Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6: 76–87.
28. Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53: 203–224.
29. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226–2230.
30. Gifford ML, Banta JA, Katari MS, Hulsmans J, Chen L, Ristova D, Tranchina D, Purugganan MD, Coruzzi GM, Birnbaum KD (2013) Plasticity regulators modulate specific root traits in discrete nitrogen environments. PLoS Genet 9: e1003760.
31. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105: 803–808.
32. Grbić V, Bleecker AB (2000) Axillary meristem development in Arabidopsis thaliana. Plant J 21: 215–223.
33. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151: 400–412.
34. Hempel F, Feldman L (1994) Bi-directional inflorescence development in Arabidopsis thaliana: acropetal initiation of flowers and basipetal initiation of paraclades. Planta 192: 276–286.
35. Jamil M, Charnikhova T, Cardoso C, Jamil T, Ueno K, Verstappen F, Asami T, Bouwmeester HJ (2011) Quantification of the relationship between strigolactones and Striga hermonthica infection in rice under varying levels of nitrogen and phosphorus. Weed Res 51: 373–385.
36. 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: 489–500.
37. Johnson X, Brcich T, Dun EA, Goussot M, Haurogné K, Beveridge CA, Rameau C (2006) Branching genes are conserved across species: genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142: 1014–1026.
38. Kebrom TH, Burson BL, Finlayson SA (2006) Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol 140: 1109–1117.
39. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155: 974–987.
40. Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A, Castaings L, Elftieh S, Major H, Renou JP, Daniel-Vedele F (2011) Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol 157: 1255–1282.
41. Lazar G, Goodman HM (2006) MAX1, a regulator of the flavonoid pathway, controls vegetative axillary bud outgrowth in Arabidopsis. Proc Natl Acad Sci USA 103: 472–476.
42. Leyser O (2009) The control of shoot branching: an example of plant information processing. Plant Cell Environ 32: 694–703.
43. Li CJ, Bangerth F (1999) Autoinhibition of indoleacetic acid transport in the shoots of two-branched pea (Pisum sativum) plants and its relationship to correlative dominance. Physiol Plant 106: 415–420.
44. Lincoln C, Britton JH, Estelle M (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2: 1071–1080.
45. 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: 751–760.
46. 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 (Lond) 106: 1019–1026.
47. Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28: 465–474.
48. López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178: 863–874.
49. Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB, Beveridge CA, Yermiyahu U, Kaplan Y, Enzer Y, et al (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol 160: 1329–1341.
50. Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37: 128–138.
51. Napoli C (1996) Highly branched phenotype of the petunia dad1-1 mutant is reversed by grafting. Plant Physiol 111: 27–37.
52. Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokininregulated development. Proc Natl Acad Sci USA 101: 8039–8044.
53. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677–684.
54. Ongaro V, Bainbridge K, Williamson L, Leyser O (2008) Interactions between axillary branches of Arabidopsis. Mol Plant 1: 388–400.
55. Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ 33: 1486–1501.
56. Prasad TK, Li X, Abdel-Rahman AM, Hosokawa Z, Cloud NP, Lamotte CE, Cline MG (1993) Does auxin play a role in the release of apical dominance by shoot inversion in Ipomoea nil? Ann Bot (Lond) 71: 223–229.
57. Prusinkiewicz P, Crawford S, Smith RS, Ljung K, Bennett T, Ongaro V, Leyser O (2009) Control of bud activation by an auxin transport switch. Proc Natl Acad Sci USA 106: 17431–17436.
58. Romano CP, Robson PR, Smith H, Estelle M, Klee H (1995) Transgenemediated auxin overproduction in Arabidopsis: hypocotyl elongation phenotype and interactions with the hy6-1 hypocotyl elongation and axr1 auxin-resistant mutants. Plant Mol Biol 27: 1071–1083.
59. Ruffel S, Krouk G, Ristova D, Shasha 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: 18524–18529.
60. Rustici G, Kolesnikov N, Brandizi M, Burdett T, Dylag M, Emam I, Farne A, Hastings E, Ison J, Keays M, et al (2013) ArrayExpress update: trends in database growth and links to data analysis tools. Nucleic Acids Res 41: D987–D990.
61. Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11: 440–448.
62. Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M (1997) Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J 11: 671–691.
63. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios- Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136: 2483–2499.
64. Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11: e1001474.
65. Snow R (1937) On the nature of correlative inhibition. New Phytol 36: 283–300.
66. Stirnberg P, Chatfield SP, Leyser HM (1999) AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiol 121: 839–847.
67. Stirnberg P, van De Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131–1141.
68. Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2: 178–186.
69. Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33: 513–520.
70. Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001) Nitrogendependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42: 85–93.
71. Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53: 971–977.
72. Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitratedependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45: 1053–1062.
73. Tamaki V, Mercier H (2007) Cytokinins and auxin communicate nitrogen availability as long-distance signal molecules in pineapple (Ananas comosus). J Plant Physiol 164: 1543–1547.
74. 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: 942–951.
75. Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51: 1118–1126
76. 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: 1494–1506.
77. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107: 4477–4482.
78. Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot (Lond) 97: 875–881.
79. Wang R, Okamoto M, Xing X, Crawford NM(2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6- phosphate, iron, and sulfate metabolism. Plant Physiol 132: 556–567.
80. Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136: 2512–2522.
81. Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222: 377–383.
82. Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312: 883.
83. Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235: 1197–1207.
84. Yoneyama K, Xie X, Kisugi T, Nomura T, Yoneyama K (2013) Nitrogen and phosphorus fertilization negatively affects strigolactone production and exudation in sorghum. Planta 238: 885–894.
85. Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227: 125–132.
86. Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225: 1031–1038.
87. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407–409.
88. Zhang H, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51: 51–59.
89. Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96: 6529–6534.
90. Zhu H, Kranz RG (2012) A nitrogen-regulated glutamine amidotransferase (GAT1_2.1) represses shoot branching in Arabidopsis. Plant Physiol 160: 1770–1780