Class i basic pentacysteine factors regulate homeobox genes involved in meristem size maintenance

Journal of Experimental Botany

Volumn 65, Issue 6, 2014, Pages 1455-1465

  Simonini, Sara ^a,b   Kater, Martin M ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

Arabidopsis; BPC; Cytokinin; Homeobox; Meristem

Indexed keywords

ARABIDOPSIS PROTEIN; CYTOKININ; HOMEODOMAIN PROTEIN; PHYTOHORMONE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; BPC; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOBOX; INFLORESCENCE; MERISTEM; MERISTEM.; METABOLISM; MUTATION; PHENOTYPE; REPORTER GENE; TRANSGENIC PLANT;

ARABIDOPSIS; BPC; CYTOKININ; HOMEOBOX; MERISTEM.;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOKININS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HOMEODOMAIN PROTEINS; INFLORESCENCE; MERISTEM; MUTATION; PHENOTYPE; PLANT GROWTH REGULATORS; PLANTS, GENETICALLY MODIFIED; TRANSCRIPTION FACTORS;

EID: 84897430357     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru003     Document Type: Article

References (66)

1. Ariel FD, Manavella PA, Dezar CA, Chan RL. 2007. The true story of the HD-Zip family Trends in Plant Science 124, 19-26.
2. Bartrina I, Otto E, Strnad M, Werner T, Schmülling T. 2011. Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23, 69-80.
3. Battaglia R, Brambilla V, Colombo L, Stuitje AR, Kater MM. 2006. Functional analysis of MADS-box genes controlling ovule development in Arabidopsis using the ethanol-inducible alc gene-expression system. Mechanisms of Development 123, 267-726.
4. Bencivenga S, Simonini S, Benkova E, Colombo L. 2012. The transcription factors BEL1 and SPL are required for cytokinin and auxin signaling during ovule development in Arabidopsis. Plant Cell 24, 2886-2897.
5. Berger N, Dubreucq B. 2012. Evolution goes GAGA: GAGA binding proteins across kingdoms. Biochimica et Biophysica Acta 1819, 863-868.
6. Berger N, Dubreucq B, Roudier F, Dubos C, Lepiniec L. 2011. Transcriptional regulation of Arabidopsis LEAFY COTYLEDON2 involves RLE, a cis-element that regulates trimethylation of histone H3 at lysine-27. Plant Cell 23, 4065-4078.
7. Botas J. 1993. Control of morphogenesis and differentiation by HOM/Hox genes. Current Opinion in Cell Biology 5, 1015-1022.
8. Brambilla V, Battaglia R, Colombo M, Masiero S, Bencivenga S, Kater MM, Colombo L. 2007. Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19, 2544-2556.
9. Buechel S, Leibfried A, To JP, Zhao Z, Andersen SU, Kieber JJ, Lohmann JU. 2010. Role of A-type ARABIDOPSIS RESPONSE REGULATORS in meristem maintenance and regeneration. European Journal of Cell Biology 89, 279-284.
10. Chan RL, Gago GM, Palena CM, Gonzalez DH. 1998. Homeoboxes in plant development. Biochimica et Biophysica Acta 1442, 1-19.
11. Clark SE, Running MP, Meyerowitz EM. 1995. CLAVATA3 is a speci'c regulator of shoot and 'oral meristem development affecting the same processes as CLAVATA1. Development 121, 2057-2067.
12. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
13. Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S. 2007. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Current Biology 17, 678-682.
14. Dewitte W, Scofield S, Alcasabas AA, et al. 2007. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proceedings of the National Academy of Sciences USA 104, 14537-14542.
15. Dreni L, Pilatone A, Yun D, Erreni S, Pajoro A, Caporali E, Zhang D, Kater MM. 2011. Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy. Plant Cell 23, 2850-2863.
16. Durbak AR, Tax FE. 2011. CLAVATA signaling pathway receptors of Arabidopsis regulate cell proliferation in fruit organ formation as well as in meristems. Genetics 189, 177-194.
17. Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T. 1996. The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. The Plant Journal 10, 967-979.
18. Favaro R Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, and Colombo L. 2003. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15, 2603-2611.
19. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM. 2009. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proceedings of the National Academy of Sciences, USA 106, 16529-16534.
20. Graba Y, Aragnol D, Pradel J. 1997. Drosophila Hox complex downstream targets and the function of homeotic genes. Bioessays 19, 379-388.
21. Grandi V, Gregis V, Kater MM. 2012. Uncovering genetic and molecular interactions among floral meristem identity genes in Arabidopsis thaliana. The Plant Journal 69, 881-893.
22. Gregis V, Andrés F, Sessa A, et al. 2013. Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis. Genome Biology 14, R56.
23. Gregis V, Sessa A, Colombo L, Kater MM. 2006. AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18, 1373-1382.
24. Gregis V, Sessa A, Colombo L, Kater MM. 2008. AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. The Plant Journal 56, 891-902.
25. Gross-Hardt R, Lenhard M, Laux T. 2002. WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes & Development 16, 1129-1138.
26. Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J. 2005. DATF: a database of Arabidopsis transcription factors. Bioinformatics 21, 2568-2569.
27. Heyl A, Ramireddy E, Brenner WG, Riefler M, Allemeersch J, Schmulling T. 2008. The transcriptional repressor ARR1-SRDX suppresses pleiotropic cytokinin activities in Arabidopsis. Plant Physiology 147, 1380-1395.
28. Hiratsu, K. Matsui K, Koyama T, Ohme-Takagi M. 2003. Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. The Plant Journal . 34, 733-739.
29. Jasinski, S., Piazza P., Craft J., Hay A., Woolley L., Rieu I., Phillips A., Hedden P, Tsiantis M. 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Current Biology 15, 1560-1565.
30. Kakimoto T. 2001. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant and Cell Physiology 42, 677-685.
31. Kanrar S, Bhattacharya M, Arthur B, Courtier J, Smith HM. 2008. Regulatory networks that function to specify flower meristems require the function of homeobox genes PENNYWISE and POUND-FOOLISH in Arabidopsis. The Plant Journal 54, 924-937.
32. Kooiker M, Airoldi CA, Losa A, Finzi L, Kater MM, Colombo L. 2005. BASIC PENTACYSTEINE1 a GA-binding protein that induces conformational changes in the regulatory region of the homeotic Arabidopsis gene SEEDSTICK. Plant Cell 17, 722-729.
33. Larkin JC, Young N, Prigge M, Marks MD. 1996. The control of trichome spacing and number in Arabidopsis. Development 122, 997-1005.
34. Laufs P, Grandjean O, Jonak C, Ki'u K, Traas J. 1998. Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10, 1375-1390.
35. Laux T, Mayer KF, Berger J, Jürgens G. 1996. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87-96.
36. Lehmann M. 2004. Anything else but GAGA: a nonhistone protein complex reshapes chromatin structure. Trends in Genetics 2, 15-22.
37. Leibfried, A., To J.P., Busch W., Stehling S., Kehle A., Demar M., Kieber JJ, Lohmann JU. 2005. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172-1175.
38. Long JA, Moan EI, Medford JI, Barton MK. 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66-69.
39. Mähönen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y. 2000. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes & Development 14, 2938-2943.
40. Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815.
41. Meister RJ, Williams LA, Monfared MM, Gallagher TL, Kraft EA, Nelson CG, Gasser CS. 2004. Definition and interaction of a positive regulatory element of the Arabidopsis INNER NO OUTER promoter. The Plant Journal 37, 426-438.
42. Monfared MM, Simon MK, Meister RJ, Roig-Villanova I, Kooiker M, Colombo L, Fletcher JC, Gasser CS. 2011. Overlapping and antagonistic activities of BASIC PENTACYSTEINE genes affect a range of developmental processes in Arabidopsis. The Plant Journal 66, 1020-1031.
43. Ori N, Eshed Y, Chuck G, Bowman JL, Hake S. 2000. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127, 5523-5532.
44. Orphanides G, LeRoy G, Chang CH, Luse DS, Reinberg D. 1998. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92, 105-116.
45. Peaucelle A, Morin H, Traas J, Laufs P. 2007. Plants expressing a miR164-resistant CUC2 gene reveal the importance of post-meristematic maintenance of phyllotaxy in Arabidopsis. Development 134, 1045-1050.
46. Pinon V, Prasad K, Grigg SP, Sanchez-Perez GF, Scheres B. 2013. Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proceedings of the National Academy of Sciences, USA 110, 1107-1112.
47. Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF. 2003. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 42, 85-88.
48. Roslan HA, Salter MG, Wood CD, et al. 2001. Characterization of the ethanol-inducible alc gene-expression system in Arabidopsis thaliana. The Plant Journal 28, 225-235.
49. Sakamoto T, Sakakibara H, Kojima M, Yamamoto Y, Nagasaki H, Inukai Y, Sato Y, Matsuoka M. 2006. Ectopic expression of KNOTTED1- like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiology 142, 54-62.
50. Sangwan I, O'Brian MR. 2002. Identification of a soybean protein that interacts with GAGA element dinucleotide repeat DNA. Plant Physiology 129, 1788-1794.
51. Santi L, Wang Y, Stile MR, et al. 2003. The GA octodinucleotide repeat binding factor BBR participates in the transcriptional regulation of the homeobox gene Bkn3. The Plant Journal 34, 813-826.
52. Schindelin J, Arganda-Carreras I, Frise E, et al. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676-682.
53. Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T. 2000. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635-644.
54. Scofield S, Dewitte W, Nieuwland J, Murray JA. 2013. The Arabidopsis homeobox gene SHOOT MERISTEMLESS has cellular and meristem-organisational roles with differential requirements for cytokinin and CYCD3 activity. The Plant Journal 75, 53-66.
55. Simonini S, Roig-Villanova I, Gregis V, Colombo B, Colombo L, Kater MM. 2012. BASIC PENTACYSTEINE proteins mediate MADS domain complex binding to the DNA for tissue-specific expression of target genes in Arabidopsis. Plant Cell 24, 4163-4172.
56. Smith HM, Hake S. 2003. The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 15, 1717-1727.
57. Takano S, Niihama M, Smith HM, Tasaka M, Aida M. 2010. gorgon, a novel missense mutation in the SHOOT MERISTEMLESS gene, impairs shoot meristem homeostasis in Arabidopsis. Plant and Cell Physiology 51, 621-634.
58. Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthélémy J, Palauqui JC. 2008. High-resolution whole-mount imaging of threedimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell 20, 1494-1503.
59. Uchida N, Townsley B, Chung KH, Sinha N. 2007. Regulation of SHOOT MERISTEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development. Proceedings of the National Academy of Sciences USA 104, 15953-15958.
60. Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, Martienssen R, Selvaraj G, Datla R. 2002. The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proceedings of the National Academy of Sciences, USA 99, 4730-4735.
61. Venglat SP, Sawhney VK. 1996. Benzylaminopurine induces phenocopies of floral meristem and organ identity mutants in wild-type Arabidopsis plants. Planta 198, 480-487.
62. Verwoerd, T.C. Dekker BM, Hoekema A. 1989. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Research 17, 2362.
63. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T. 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15, 2532-2550.
64. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N. 2005. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Current Biology 15, 1566-1571.
65. Yoshida S, Mandel T, Kuhlemeier C. 2011. Stem cell activation by light guides plant organogenesis. Genes & Development 25, 1439-1450.
66. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU. 2010. Hormonal control of the shoot stem-cell niche. Nature 465, 1089-1092.