Modulation of Arabidopsis and monocot root architecture by CLAVATA3/EMBRYO SURROUNDING REGION 26 peptide

Journal of Experimental Botany

Volumn 66, Issue 17, 2015, Pages 5229-5243

  Czyzewicz, Nathan ^a   Shi, Chun Lin ^b   Vu, Lam Dai ^c,d   Van De Cotte, Brigitte ^c,d   Hodgman, Charlie ^a   Butenko, Melinka A ^b   Smet, Ive De ^a,c,d  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF OSLO   (Norway)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

Arabidopsis thaliana; auxin; Brachypodium distachyon; CLE26; root; wheat

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRACHYPODIUM DISTACHYON; TRITICUM AESTIVUM;

ARABIDOPSIS PROTEIN; CLE26 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; BRACHYPODIUM; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYLOGENY; PLANT ROOT; WHEAT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRACHYPODIUM; GENE EXPRESSION REGULATION, PLANT; PHYLOGENY; PLANT ROOTS; TRITICUM;

EID: 84939608298     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv360     Document Type: Article

References (77)

1. Araya T, Miyamoto M, Wibowo J, et al. 2014. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proceedings of the National Academy of Sciences, USA 111, 2029-2034.
2. 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.
3. Betsuyaku S, Sawa S, Yamada M. 2011. The function of the CLE peptides in plant development and plant-microbe interactions. Arabidopsis Book 9, e0149.
4. Bidadi H, Matsuoka K, Sage-Ono K, et al. 2014. CLE6 expression recovers gibberellin deficiency to promote shoot growth in Arabidopsis. The Plant Journal 78, 241-252.
5. Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benková E, Mähönen Ari P, Helariutta Y. 2011. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Current Biology 21, 917-926.
6. Brunoud G, Wells DM, Oliva M, et al. 2012. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103-106.
7. Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM. 2009. Plant peptides in signalling: looking for new partners. Trends in Plant Science 14, 255-263.
8. Butenko MA, Wildhagen M, Albert M, Jehle A, Kalbacher H, Aalen RB, Felix G. 2014. Tools and strategies to match peptide-ligand receptor pairs. The Plant Cell 26, 1838-1847.
9. Casamitjana-Martinez E, Hofhuis HF, Xu J, Liu CM, Heidstra R, Scheres B. 2003. Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Current Biology 13, 1435-1441.
10. Clark SE, Running MP, Meyerowitz EM. 1995. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057-2067.
11. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Research 14, 1188-1190.
12. Czyzewicz N, Wildhagen M, Cattaneo P, et al. 2015. Antagonistic peptide technology revisited. Journal of Experimental Biology 66, 5367-5374.
13. Czyzewicz N, Yue K, Beeckman T, De Smet I. 2013. Message in a bottle: small signalling peptide outputs during growth and development. Journal of Experimental Biology 64, 5281-5296.
14. Davière J-M, Achard P. 2013. Gibberellin signaling in plants. Development 140, 1147-1151.
15. Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS. 2013. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptorlike kinase BAM3. Proceedings of the National Academy of Sciences, USA 110, 7074-7079.
16. De Smet I. 2012. Lateral root initiation: one step at a time. New Phytologist 193, 867-873.
17. De Smet I, Signora L, Beeckman T, Inze D, Foyer CH, Zhang H. 2003. An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. The Plant Journal 33, 543-555.
18. De Smet I, Tetsumura T, De Rybel B, et al. 2007. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134, 681-690.
19. Ding Z, De Smet I. 2013. Localised ABA signalling mediates root growth plasticity. Trends in Plant Science 18, 533-535.
20. Duan L, Dietrich D, Ng CH, Chan PM, Bhalerao R, Bennett MJ, Dinneny JR. 2013. Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. The Plant Cell 25, 324-341.
21. Dunbrack RL Jr. 2002. Rotamer libraries in the 21st century. Current Opinion in Structural Biology 12, 431-440.
22. El-Showk S, Ruonala R, Helariutta Y. 2013. Crossing paths: cytokinin signalling and crosstalk. Development 140, 1373-1383.
23. Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu CM. 2005. The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. The Plant Cell 17, 2542-2553.
24. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911-1914.
25. Funayama-Noguchi S, Noguchi K, Yoshida C, Kawaguchi M. 2011. Two CLE genes are induced by phosphate in roots of Lotus japonicus. Journal of Plant Research 124, 155-163.
26. Geier F, Lohmann JU, Gerstung M, Maier AT, Timmer J, Fleck C. 2008. A quantitative and dynamic model for plant stem cell regulation. PLoS One 3, e3553.
27. Goodstein DM, Shu S, Howson R, et al. 2011. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178-D1186.
28. Gruber BD, Giehl RF, Friedel S, von Wiren N. 2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163, 161-179.
29. Guo Y, Han L, Hymes M, Denver R, Clark SE. 2010. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. The Plant Journal 63, 889-900.
30. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8, R19.
31. Hirakawa Y, Shinohara H, Kondo Y, et al. 2008. Non-cellautonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proceedings of the National Academy of Sciences, USA 105, 15208-15213.
32. Hobe M, Muller R, Grunewald M, Brand U, Simon R. 2003. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Development Genes and Evolution 213, 371-381.
33. Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H. 2006. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313, 842-845.
34. Jun J, Fiume E, Roeder AHK, et al. 2010. Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiology 154, 1721-1736.
35. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4, 363-371.
36. Kinoshita A, Nakamura Y, Sasaki E, Kyozuka J, Fukuda H, Sawa S. 2007. Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant and Cell Physiology 48, 1821-1825.
37. Kondo T, Nakamura T, Yokomine K, Sakagami Y. 2008. Dual assay for MCLV3 activity reveals structure-activity relationship of CLE peptides. Biochemical and Biophysical Research Communications 377, 312-316.
38. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y. 2006. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313, 845-848.
39. Kurup S, Runions J, Kohler U, Laplaze L, Hodge S, Haseloff J. 2005. Marking cell lineages in living tissues. The Plant Journal 42, 444-453.
40. Lavenus J, Goh T, Roberts I, et al. 2013. Lateral root development in Arabidopsis: fifty shades of auxin. Trends in Plant Science 18, 450-458.
41. Lee JY, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN. 2006 Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proceedings of the National Academy of Sciences, USA 103, 6055-6060.
42. Lim CW, Lee YW, Lee SC, Hwang CH. 2014. Nitrate inhibits soybean nodulation by regulating expression of CLE genes. Plant Science 229, 1-9.
43. Malamy JE, Benfey PN. 1997. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124, 33-44.
44. Marhavy P, Duclercq J, Weller B, et al. 2014. Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Current Biology 24, 1031-1037.
45. Matsubayashi Y. 2011. Post-translational modifications in secreted peptide hormones in plants. Plant and Cell Physiology 52, 5-13.
46. Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y. 2010 Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329, 1065-1067.
47. Meng L, Feldman LJ. 2010. CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis. Planta 232, 1061-1074.
48. Miyawaki K, Tabata R, Sawa S. 2013. Evolutionarily conserved CLE peptide signaling in plant development, symbiosis, and parasitism. Current Opinion in Plant Biology 16, 598-606.
49. Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S. 2012. Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. The Plant Journal 70, 367-376.
50. Murphy E, De Smet I. 2014. Understanding the RALF family: a tale of many species. Trends in Plant Science 19, 664-671.
51. Murphy E, Smith S, De Smet I. 2012. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. The Plant Cell 24, 3198-3217.
52. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 1150083.
53. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y. 2009 A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nature Chemical Biology 5, 578-580.
54. 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 and Cell Physiology 50, 67-77.
55. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. 2007 ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. The Plant Cell 19, 118-130.
56. Parizot B, Laplaze L, Ricaud L, et al. 2008. Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiology 146, 140-148.
57. Parizot B, Roberts I, Raes J, Beeckman T, De Smet I. 2012. In silico analyses of pericycle cell populations reinforce their relation with associated vasculature in Arabidopsis. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 1479-1488.
58. Pearce G, Moura DS, Stratmann J, Ryan CA. 2001. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proceedings of the National Academy of Sciences, USA 98, 12843-12847.
59. Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ. 2009. Arabidopsis lateral root development: an emerging story. Trends in Plant Science 14, 399-408.
60. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25, 1605-1612.
61. Reid DE, Ferguson BJ, Gresshoff PM. 2011. Inoculation-and nitrateinduced CLE peptides of soybean control NARK-dependent nodule formation. Molecular Plant-Microbe Interactions 24, 606-618.
62. Rodriguez-Villalon A, Gujas B, Kang YH, Breda AS, Cattaneo P, Depuydt S, Hardtke CS. 2014. Molecular genetic framework for protophloem formation. Proceedings of the National Academy of Sciences, USA 111, 11551-11556.
63. Rodriguez-Villalon A, Gujas B, van Wijk R, Munnik T, Hardtke CS. 2015. Primary root protophloem differentiation requires balanced phosphatidylinositol-4-5-biphosphate levels and systemically affects root branching. Development 142, 1437-1446.
64. Sawa S, Kinoshita A, Nakanomyo I, Fukuda H. 2006. CLV3/ESRrelated (CLE) peptides as intercellular signaling molecules in plants. Chemical Record 6, 303-310.
65. Schindelin J, Arganda-Carreras I, Frise E, et al. 2012. Fiji: an opensource platform for biological-image analysis. Nature Methods 9, 676-682.
66. Sharma V, Ramirez J, Fletcher J. 2003. The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins. Plant Molecular Biology 51, 415-425.
67. Shinohara H, Matsubayashi Y. 2013. Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity. Plant and Cell Physiology 54, 369-374.
68. Smith S, De Smet I. 2012. Root system architecture: insights from Arabidopsis and cereal crops. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 1441-1452.
69. Song XF, Guo P, Ren SC, Xu TT, Liu CM. 2013. Antagonistic peptide technology for functional dissection of CLV3/ESR genes in Arabidopsis. Plant Physiology 161, 1076-1085.
70. Stahl Y, Grabowski S, Bleckmann A, et al. 2013. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Current Biology 23, 362-371.
71. Strabala TJ, O'Donnell PJ, Smit A-M, et al. 2006. Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiology 140, 1331-1344.
72. Tian H, De Smet I, Ding Z. 2014. Shaping a root system: regulating lateral versus primary root growth. Trends in Plant Science 19, 426-431.
73. Vanstraelen M, Benkova E. 2012. Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology 28, 463-487.
74. Vernoux T, Brunoud G, Farcot E, et al. 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Molecular Systems Biology 7, 508.
75. Wang G, Fiers M. 2010. CLE peptide signaling during plant development. Protoplasma 240, 33-43.
76. Yoon GM, Kieber JJ. 2013. 1-Aminocyclopropane-1-carboxylic acid as a signalling molecule in plants. AoB Plants 5, plt017.
77. Zhao C, Craig JC, Petzold HE, Dickerman AW, Beers EP. 2005 The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiology 138, 803-818.