A bHLH-Based Feedback Loop Restricts Vascular Cell Proliferation in Plants

Developmental Cell

Volumn 35, Issue 4, 2015, Pages 432-443

  Vera Sirera, Francisco ^a   De Rybel, Bert ^b,d   Úrbez, Cristina ^a   Kouklas, Evangelos ^b,e   Pesquera, Marta ^a   Álvarez Mahecha, Juan Camilo ^a   Minguet, Eugenio G ^a   Tuominen, Hannele ^c   Carbonell, Juan ^a   Borst, Jan Willem ^b   Weijers, Dolf ^b   Blázquez, Miguel A ^a  

^a UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UMEÅ UNIVERSITY   (Sweden)

^d GHENT UNIVERSITY   (Belgium)

^e MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; LONESOME HIGHWAY; PHYTOHORMONE; PROTEIN ACAULIS5; PROTEIN SACL51; TARGET OF MONOPTEROS 5; THERMOSPERMINE SYNTHASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ACAULIS5 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; LHW PROTEIN, ARABIDOPSIS; MESSENGER RNA; SAC51 PROTEIN, ARABIDOPSIS; TARGET OF MP 5 PROTEIN, ARABIDOPSIS; TRANSACTIVATOR PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; CELL DIVISION; CELL PROLIFERATION; COMPLEX FORMATION; DIMERIZATION; FEEDBACK SYSTEM; GENE ACTIVATION; GENE EXPRESSION; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT TISSUE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; TISSUE GROWTH; TRANSLATION REGULATION; VASCULAR TISSUE; ANTAGONISTS AND INHIBITORS; ARABIDOPSIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT ROOT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC PLANT; XYLEM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANS-ACTIVATORS; XYLEM;

EID: 84961658259     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.10.022     Document Type: Article

References (47)

1. Alabadí D., Gallego-Bartolomé J., Orlando L., García-Cárcel L., Rubio V., Martínez C., Frigerio M., Iglesias-Pedraz J.M., Espinosa A., Deng X.W., Blázquez M.A. Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J. 2008, 53:324-335.
2. Baima S., Forte V., Possenti M., Peñalosa A., Leoni G., Salvi S., Felici B., Ruberti I., Morelli G. Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module. Mol. Plant 2014, 7:1006-1025.
3. Bücherl C.A., van Esse G.W., Kruis A., Luchtenberg J., Westphal A.H., Aker J., van Hoek A., Albrecht C., Borst J.W., de Vries S.C. Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol. 2013, 162:1911-1925.
4. Carbonell-Bejerano P., Urbez C., Carbonell J., Granell A., Perez-Amador M.A. A fertilization-independent developmental program triggers partial fruit development and senescence processes in pistils of Arabidopsis. Plant Physiol. 2010, 154:163-172.
5. Chickarmane V.S., Gordon S.P., Tarr P.T., Heisler M.G., Meyerowitz E.M. Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. USA 2012, 109:4002-4007.
6. Clay N.K., Nelson T. Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol. 2005, 138:767-777.
7. De Rybel B., Möller B., Yoshida S., Grabowicz I., Barbier de Reuille P., Boeren S., Smith R.S., Borst J.W., Weijers D. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev. Cell 2013, 24:426-437.
8. De Rybel B., Adibi M., Breda A.S., Wendrich J.R., Smit M.E., Novák O., Yamaguchi N., Yoshida S., Van Isterdael G., Palovaara J., et al. Plant development. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 2014, 345:1255215.
9. Edgar R., Domrachev M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
10. Etchells J.P., Mishra L.S., Kumar M., Campbell L., Turner S.R. Wood Formation in Trees Is Increased by Manipulating PXY-Regulated Cell Division. Curr. Biol. 2015, 25:1050-1055.
11. Fisher K., Turner S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 2007, 17:1061-1066.
12. Hanzawa Y., Takahashi T., Komeda Y. ACL5: an Arabidopsis gene required for internodal elongation after flowering. Plant J. 1997, 12:863-874.
13. Hanzawa Y., Takahashi T., Michael A.J., Burtin D., Long D., Pineiro M., Coupland G., Komeda Y. ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J. 2000, 19:4248-4256.
14. Hayden C.A., Jorgensen R.A. Identification of novel conserved peptide uORF homology groups in Arabidopsis and rice reveals ancient eukaryotic origin of select groups and preferential association with transcription factor-encoding genes. BMC Biol. 2007, 5:32.
15. Hirakawa Y., Shinohara H., Kondo Y., Inoue A., Nakanomyo I., Ogawa M., Sawa S., Ohashi-Ito K., Matsubayashi Y., Fukuda H. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl. Acad. Sci. USA 2008, 105:15208-15213.
16. Hirakawa Y., Kondo Y., Fukuda H. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 2010, 22:2618-2629.
17. Imai A., Hanzawa Y., Komura M., Yamamoto K.T., Komeda Y., Takahashi T. The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 2006, 133:3575-3585.
18. Imai A., Komura M., Kawano E., Kuwashiro Y., Takahashi T. A semi-dominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. Plant J. 2008, 56:881-890.
19. Ito Y., Nakanomyo I., Motose H., Iwamoto K., Sawa S., Dohmae N., Fukuda H. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 2006, 313:842-845.
20. Jouannet V., Brackmann K., Greb T. (Pro)cambium formation and proliferation: two sides of the same coin?. Curr. Opin. Plant Biol. 2015, 23:54-60.
21. Kakehi J., Kuwashiro Y., Motose H., Igarashi K., Takahashi T. Norspermine substitutes for thermospermine in the control of stem elongation in Arabidopsis thaliana. FEBS Lett. 2010, 584:3042-3046.
22. Kakehi J., Kawano E., Yoshimoto K., Cai Q., Imai A., Takahashi T. Mutations in ribosomal proteins, RPL4 and RACK1, suppress the phenotype of a thermospermine-deficient mutant of Arabidopsis thaliana. PLoS ONE 2015, 10:e0117309.
23. Knott J.M., Römer P., Sumper M. Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett. 2007, 581:3081-3086.
24. Llavata-Peris C., Lokerse A., Möller B., De Rybel B., Weijers D. Imaging of phenotypes, gene expression, and protein localization during embryonic root formation in Arabidopsis. Methods Mol. Biol. 2013, 959:137-148.
25. Locascio A., Blázquez M.A., Alabadí D. Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr. Biol. 2013, 23:804-809.
26. Lucas W.J., Groover A., Lichtenberger R., Furuta K., Yadav S.-R., Helariutta Y., He X.-Q., Fukuda H., Kang J., Brady S.M., et al. The plant vascular system: evolution, development and functions. J. Integr. Plant Biol. 2013, 55:294-388.
27. Mähönen A.P., Bonke M., Kauppinen L., Riikonen M., Benfey P.N., Helariutta Y. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 2000, 14:2938-2943.
28. Mähönen A.P., Bishopp A., Higuchi M., Nieminen K.M., Kinoshita K., Törmäkangas K., Ikeda Y., Oka A., Kakimoto T., Helariutta Y. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 2006, 311:94-98.
29. Marín-de la Rosa N., Sotillo B., Miskolczi P., Gibbs D.J., Vicente J., Carbonero P., Oñate-Sánchez L., Holdsworth M.J., Bhalerao R., Alabadí D., Blázquez M.A. Large-scale identification of gibberellin-related transcription factors defines group VII ETHYLENE RESPONSE FACTORS as functional DELLA partners. Plant Physiol. 2014, 166:1022-1032.
30. Marín-de la Rosa N., Pfeiffer A., Hill K., Locascio A., Bhalerao R.P., Miskolczi P., Grønlund A.L., Wanchoo-Kohli A., Thomas S.G., Bennett M.J., et al. Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins. PLoS Genet. 2015, 11:e1005337.
31. Matsuhara S., Jingu F., Takahashi T., Komeda Y. Heat-shock tagging: a simple method for expression and isolation of plant genome DNA flanked by T-DNA insertions. Plant J. 2000, 22:79-86.
32. Milhinhos A., Prestele J., Bollhöner B., Matos A., Vera-Sirera F., Rambla J.L., Ljung K., Carbonell J., Blázquez M.A., Tuominen H., Miguel C.M. Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem. Plant J. 2013, 75:685-698.
33. Minguet E.G., Vera-Sirera F., Marina A., Carbonell J., Blázquez M.A. Evolutionary diversification in polyamine biosynthesis. Mol. Biol. Evol. 2008, 25:2119-2128.
34. Muñiz L., Minguet E.G., Singh S.K., Pesquet E., Vera-Sirera F., Moreau-Courtois C.L., Carbonell J., Blázquez M.A., Tuominen H. ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 2008, 135:2573-2582.
35. Nieminen K., Blomster T., Helariutta Y., Mähönen A.P. Vascular Cambium Development. Arabidopsis Book 2015, 13:e0177.
36. Ohashi-Ito K., Bergmann D.C. Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY. Development 2007, 134:2959-2968.
37. Ohashi-Ito K., Matsukawa M., Fukuda H. An atypical bHLH transcription factor regulates early xylem development downstream of auxin. Plant Cell Physiol. 2013, 54:398-405.
38. Ohashi-Ito K., Saegusa M., Iwamoto K., Oda Y., Katayama H., Kojima M., Sakakibara H., Fukuda H. A bHLH complex activates vascular cell division via cytokinin action in root apical meristem. Curr. Biol. 2014, 24:2053-2058.
39. Pires N., Dolan L. Origin and diversification of basic-helix-loop-helix proteins in plants. Mol. Biol. Evol. 2010, 27:862-874.
40. Reed J.W. Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 2001, 6:420-425.
41. Schlereth A., Möller B., Liu W., Kientz M., Flipse J., Rademacher E.H., Schmid M., Jürgens G., Weijers D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 2010, 464:913-916.
42. Sieburth L.E. Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol. 1999, 121:1179-1190.
43. Takano A., Kakehi J., Takahashi T. Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol. 2012, 53:606-616.
44. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
45. Tokunaga H., Kojima M., Kuroha T., Ishida T., Sugimoto K., Kiba T., Sakakibara H. Arabidopsis lonely guy (LOG) multiple mutants reveal a central role of the LOG-dependent pathway in cytokinin activation. Plant J. 2012, 69:355-365.
46. Toledo-Ortiz G., Huq E., Quail P.H. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 2003, 15:1749-1770.
47. Tong W., Yoshimoto K., Kakehi J., Motose H., Niitsu M., Takahashi T. Thermospermine modulates expression of auxin-related genes in Arabidopsis. Front. Plant Sci. 2014, 5:94.