Phloem-Mobile Aux/IAA Transcripts Target to the Root Tip and Modify Root Architecture

Journal of Integrative Plant Biology

Volumn 54, Issue 10, 2012, Pages 760-772

  Notaguchi, Michitaka ^a,c   Wolf, Shmuel ^b   Lucas, William J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

Arabidopsis; AUX IAA; Grafting; Lateral root development; Phloem mobile transcript

Indexed keywords

ARABIDOPSIS PROTEIN; IAA18 PROTEIN, ARABIDOPSIS; IAA28 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

EXPERIMENTAL STUDY; GRAFTING; LABORATORY METHOD; NUTRIENT UPTAKE; PHLOEM; PLANT; RNA;

ARABIDOPSIS; ARTICLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; PHLOEM; PLANT ROOT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; MERISTEM; PHLOEM; PLANT ROOTS; TRANSCRIPTION FACTORS;

EID: 84867361055     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2012.01155.x     Document Type: Article

References (66)

1. Allen J, Baker D (1980) Free tryptophan and indole-3-acetic acid levels in the leaves and vascular pathways of Ricinus communis. L. Planta 148, 69-74.
2. Aoyama T, Chua NH (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605-612.
3. Atkins CA, Smith PM, Rodriguez-Medina C (2011) Macromolecules in phloem exudates - A review. Protoplasma 248, 165-172.
4. Banerjee AK, Chatterjee M, Yu Y, Suh SG, Miller WA, Hannapel DJ (2006) Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18, 3443-3457.
5. Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103-106.
6. Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Genet. 43, 265-285.
7. Chhun T, Uno Y, Taketa S, Azuma T, Ichii M, Okamoto T, Tsurumi S (2007) Saturated humidity accelerates lateral root development in rice (Oryza sativa L.) seedlings by increasing phloem-based auxin transport. J. Exp. Bot. 58, 1695-1704.
8. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
9. Corbesier L, Prinsen E, Jacqmard A, Lejeune P, Van Onckelen H, Périlleux C, Bernier G (2003) Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition. J. Exp. Bot. 54, 2511-2517.
10. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033.
11. Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol. 5, e222.
12. De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, Möller B, Wilson M, Holman T, Van Isterdael G, Brunoud G, Vuylsteke M, Vernoux T, De Veylder L, Inzé D, Weijers D, Bennett MJ, Beeckman T (2010) A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 20, 1697-1706.
13. De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inzé D, Bennett MJ, Beeckman T (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134, 681-690.
14. Endo M, Nakamura S, Araki T, Mochizuki N, Nagatani A (2005) Phytochrome B in the mesophyll delays flowering by suppressing FLOWERING LOCUS T expression in Arabidopsis vascular bundles. Plant Cell 17, 1941-1952.
15. Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29, 153-168.
16. Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol. Biol. 69, 437-449.
17. Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z, Min J, Guo X, Murat F, Ham BK, Zhang Z, Gao S, Huang M, Xu Y, Zhong S, Bombarely A, Mueller LA, Zhao H, He H, Zhang Y, Zhang Z, Huang S, Tan T, Pang E, Lin K, Hu Q, Kuang H, Ni P, Wang B, Liu J, Kou Q, Hou W, Zou X, Jiang J, Gong G, Klee K, Schoof H, Huang Y, Hu X, Dong S, Liang D, Wang J, Wu K, Xia Y, Zhao X, Zheng Z, Xing M, Liang X, Huang B, Lv T, Wang J, Yin Y, Yi H, Li R, Wu M, Levi A, Zhang X, Giovannoni JJ, Wang J, Li Y, Fei Z, Xu Y (2012) The draft genome of watermelon (Citrullus lunatus) and resequencing of 20 diverse accessions. Nat. Genet 44, In Press.
18. Haywood V, Yu TS, Huang NC, Lucas WJ (2005) Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J. 42, 49-68.
19. Hoad GV (1995) Transport of hormones in the phloem of higher plants. Plant Growth Regul. 16, 173-182.
20. Hsu CH, Lin SS, Liu FL, Su WC, Yeh SD (2004) Oral administration of a mite allergen expressed by zucchini yellow mosaic virus in cucurbit species downregulates allergen-induced airway inflammation and IgE synthesis. J. Allergy Clin. Immunol. 113, 1079-1085.
21. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P, Ren Y, Zhu H, Li J, Lin K, Jin W, Fei Z, Li G, Staub J, Kilian A, van der Vossen EA, Wu Y, Guo J, He J, Jia Z, Tian G, Lu Y, Ruan J, Qian W, Wang M, Huang Q, Li B, Xuan Z, Cao J, Asan, Wu Z, Zhang J, Cai Q, Bai Y, Zhao B, Han Y, Li Y, Li X, Wang S, Shi Q, Liu S, Cho WK, Kim JY, Xu Y, Heller-Uszynska K, Miao H, Cheng Z, Zhang S, Wu J, Yang Y, Kang H, Li M, Liang H, Ren X, Shi Z, Wen M, Jian M, Yang H, Zhang G, Yang Z, Chen R, Ma L, Liu H, Zhou Y, Zhao J, Fang X, Fang L, Liu D, Zheng H, Zhang Y, Qin N, Li Z, Yang G, Yang S, Bolund L, Kristiansen K, Li S, Zhang X, Wang J, Sun R, Zhang B, Jiang S, Du Y (2009) The genome of the cucumber, Cucumis sativus L. Nat. Genet. 41, 1275-1281.
22. Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11, 309-322.
23. Jager CE, Symons GM, Glancy NE, Reid JB, Ross JJ (2007) Evidence that the mature leaves contribute auxin to the immature tissues of pea (Pisum sativum L.). Planta 226, 361-368.
24. Kamboj JS, Blake PS, Baker DA (1998) Cytokinins in the vascular sap of Ricinus communis. Plant Growth Regul. 25, 123-126.
25. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286, 1962-1965.
26. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
27. Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J. Exp. Bot. 59, 85-92.
28. Kieffer M, Neve J, Kepinski S (2010) Defining auxin response contexts in plant development. Curr. Opin. Plant Biol. 13, 12-20.
29. Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science. 293, 287-289.
30. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960-1962.
31. Kotogány E, Dudits D, Horváth GV, Ayaydin F (2010) A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods 6, 5.
32. Kudo T, Kiba T, Sakakibara H (2010) Metabolism and long-distance translocation of cytokinins. J. Integr. Plant Biol. 52, 53-60.
33. Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root meristems is a two-stage process. Development 121, 3303-3310.
34. Le Hir R, Beneteau J, Bellini C, Vilaine F, Dinant S (2008) Gene expression profiling: Keys for investigating phloem functions. Trends Plant Sci. 13, 273-280.
35. Lin M-K, Belanger H, Lee YJ, Varkonyi-Gasic E, Taoka K, Miura E, Xoconostle-Cázares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ, Lucas WJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19, 1488-1506.
36. Lough TJ, Lucas WJ (2006) Integrative plant biology: Role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol. 57, 203-232.
37. Ma Y, Miura E, Ham BK, Cheng HW, Lee YJ, Lucas WJ (2010) Pumpkin eIF5A isoforms interact with components of the translational machinery in the cucurbit sieve tube system. Plant J. 64, 536-550.
38. 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.
39. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872-875.
40. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329, 1306-1311.
41. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34-41.
42. NASC, the European Arabidopsis Stock Centre GAL4-GFP Enhancer-trap lines [online] Available at: [Accessed 22 June 2012.
43. Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
44. Nibau C, Gibbs DJ, Coates JC (2008) Branching out in new directions: The control of root architecture by lateral root formation. New Phytol. 179, 595-614.
45. Notaguchi M, Daimon Y, Abe M, Araki T (2009) Adaptation of a seedling micro-grafting technique to the study of long-distance signaling in flowering of Arabidopsis thaliana. J. Plant Res. 122, 201-214.
46. Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S (2007) Characterization of phloem-sap transcription profile in melon plants. J. Exp. Bot. 58, 3645-3656.
47. Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K (2009) The evolution of nuclear auxin signalling. BMC Evol. Biol. 9, 126.
48. Ploense SE, Wu MF, Nagpal P, Reed JW (2009) A gain-of-function mutation in IAA18 alters Arabidopsis embryonic apical patterning. Development 136, 1509-1517.
49. Péret B, Larrieu A, Bennett MJ (2009) Lateral root emergence: A difficult birth. J. Exp. Bot. 60, 3637-3643.
50. Rim Y, Jung JH, Chu H, Cho WK, Kim SW, Hong JC, Jackson D, Datla R, Kim JY (2009) A non-cell-autonomous mechanism for the control of plant architecture and epidermal differentiation involves intercellular trafficking of BREVIPEDICELLUS protein. Funct. Plant Biol. 36, 280-289.
51. Rocher F, Chollet JF, Jousse C, Bonnemain JL (2006) Salicylic acid, an ambimobile molecule exhibiting a high ability to accumulate in the phloem. Plant Physiol. 141, 1684-1693.
52. Rogg LE, Bartel B (2001) Auxin signaling: Derepression through regulated proteolysis. Dev. Cell 1, 595-604.
53. Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13, 465-480.
54. Samson F, Brunaud V, Balzergue S, Dubreucq B, Lepiniec L, Pelletier G, Caboche M, Lecharny A (2002) FLAGdb/FST: A database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res. 30, 94-97.
55. Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 139, 701-712.
56. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316, 1033-1036.
57. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. USA 104, 1075-1080.
58. Turgeon R, Wolf S (2009) Phloem transport: Cellular pathways and molecular trafficking. Annu. Rev. Plant Biol. 60, 207-221.
59. Turnbull C (2011) Long-distance regulation of flowering time. J. Exp. Bot. 62, 4399-4413.
60. Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255-262.
61. UC Davis Controlled Environment Facility, [online] Available at: [Accessed 22 July 2012.
62. Uehara T, Okushima Y, Mimura T, Tasaka M, Fukaki H (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol. 49, 1025-1038.
63. Vanneste S, Friml J (2009) Auxin: A trigger for change in plant development. Cell 136, 1005-1016.
64. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47, 177-206.
65. Wigge PA (2011) FT, a mobile developmental signal in plants. Curr. Biol. 21, R374-378.
66. Xoconostle-Cázares B, Xiang Y, Ruiz-Medrano R, Wang HL, Monzer J, Yoo BC, McFarland KC, Franceschi VR, Lucas WJ (1999) Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283, 94-98.