Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases

Development (Cambridge)

Volumn 142, Issue 6, 2015, Pages 1043-1049

  Nimchuk, Zachary L ^a,b   Zhou, Yun ^a   Tarr, Paul T ^a   Peterson, Brenda A ^b   Meyerowitz, Elliot M ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; CLV1; Plant development; Receptor kinase; Stem cells

Indexed keywords

BARELY ANY MERISTEM 1 RECEPTOR KINASE; BARELY ANY MERISTEM 2 RECEPTOR KINASE; BARELY ANY MERISTEM 3 RECEPTOR KINASE; CLAVATA1 RECEPTOR KINASE; CLAVATA3 RECEPTOR KINASE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; WUSCHEL PROTEIN; ARABIDOPSIS PROTEIN; BAM1 PROTEIN, ARABIDOPSIS; BAM2 PROTEIN, ARABIDOPSIS; BAM3 PROTEIN, ARABIDOPSIS; CLV1 PROTEIN, ARABIDOPSIS; CLV3 PROTEIN, ARABIDOPSIS; HOMEODOMAIN PROTEIN; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; WUSCHEL PROTEIN, ARABIDOPSIS;

APICAL MERISTEM; ARABIDOPSIS; ARTICLE; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; FLOWER; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; MERISTEM; NONHUMAN; PHENOTYPE; PLANT CELL; PLANT GENE; PLANT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR GENE; SHOOT; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION REGULATION; CONFOCAL MICROSCOPY; CROSS BREEDING; CYTOLOGY; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; GENOTYPE; METABOLISM; MUTATION; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL PROLIFERATION; CROSSES, GENETIC; GENE EXPRESSION REGULATION, PLANT; GENETIC VECTORS; GENOTYPE; HOMEODOMAIN PROTEINS; MICROSCOPY, CONFOCAL; MUTATION; PLANTS, GENETICALLY MODIFIED; PROTEIN-SERINE-THREONINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84930531507     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.119677     Document Type: Article

References (42)

1. Barrell, P. J. and Conner, A. J. (2006). Minimal T-DNA vectors suitable for agricultural deployment of transgenic plants. Biotechniques 41, 708-710.
2. Barton, M. K. (2009). Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev. Biol. 341, 95-113.
3. Brady, S. M., Orlando, D. A., Lee, J.-Y., Wang, J. Y., Koch, J., Dinneny, J. R., Mace, D., Ohler, U. and Benfey, P. N. (2007). A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318, 801-806.
4. Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. and Simon, R. (2000). Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617-619.
5. Brand, U., Grünewald, M., Hobe, M. and Simon, R. (2002). Regulation of CLV3 expression by two homeobox genes in Arabidopsis. Plant Physiol. 129, 565-575.
6. Briggs, G. C., Osmont, K. S., Shindo, C., Sibout, R. and Hardtke, C. S. (2006). Unequal genetic redundancies in Arabidopsis–a neglected phenomenon? Trends Plant Sci. 11, 492-498.
7. Busch, W., Miotk, A., Ariel, F. D., Zhao, Z., Forner, J., Daum, G., Suzaki, T., Schuster, C., Schultheiss, S. J., Leibfried, A. et al. (2010). Transcriptional control of a plant stem cell niche. Dev. Cell 18, 841-853.
8. Chickarmane, V. S., Gordon, S. P., Tarr, P. T., Heisler, M. G. and Meyerowitz, E. M. (2012). Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. USA 109, 4002-4007.
9. Clark, S. E., Running, M. P. and Meyerowitz, E. M. (1993). CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119, 397-418.
10. Clark, S. E., Running, M. P. and Meyerowitz, E. M. (1995). CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057-2067.
11. Clark, S. E., Williams, R. W. and Meyerowitz, E. M. (1997). The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575-585.
12. Clough, S. J. and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
13. Cutler, S. R., Ehrhardt, D. W., Griffitts, J. S. and Somerville, C. R. (2000). Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. USA 97, 3718-3723.
14. Depuydt, S., Rodriguez-Villalon, A., Santuari, L., Wyser-Rmili, C., Ragni, L. and Hardtke, C. S. (2013). Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proc. Natl. Acad. Sci. USA 110, 7074-7079.
15. DeYoung, B. J. and Clark, S. E. (2008). BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180, 895-904.
16. DeYoung, B. J., Bickle, K. L., Schrage, K. J., Muskett, P., Patel, K. and Clark, S. E. (2006). The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinaselike proteins are required for meristem function in Arabidopsis. Plant J. 45, 1-16.
17. Dievart, A., Dalal, M., Tax, F. E., Lacey, A. D., Huttly, A., Li, J. and Clark, S. E. (2003). CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell 15, 1198-1211.
18. Fletcher, J. C., Brand, U., Running, M. P., Simon, R. and Meyerowitz, E. M. (1999). Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911-1914.
19. Gordon, S. P., Chickarmane, V. S., Ohno, C. and Meyerowitz, E. M. (2009). Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. USA 106, 16529-16534.
20. Green, K. A., Prigge, M. J., Katzman, R. B. and Clark, S. E. (2005). CORONA, a member of the class III homeodomain leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 17, 691-704.
21. Guo, Y., Han, L., Hymes, M., Denver, R. and Clark, S. E. (2010). CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889-900.
22. Kafri, R., Springer, M. and Pilpel, Y. (2009). Genetic redundancy: new tricks for old genes. Cell 136, 389-392.
23. Kinoshita, A., Betsuyaku, S., Osakabe, Y., Mizuno, S., Nagawa, S., Stahl, Y., Simon, R., Yamaguchi-Shinozaki, K., Fukuda, H. and Sawa, S. (2010). RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911-3920.
24. Kondo, T., Sawa, S., Kinoshita, A., Mizuno, S., Kakimoto, T., Fukuda, H. and Sakagami, Y. (2006). A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313, 845-848.
25. Lee, J. Y., Colinas, J., Wang, J. Y., Mace, D., Ohler, U. and Benfey, P. N. (2006). Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 103, 6055-606.
26. Mayer, K. F. X., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G. and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815.
27. Muller, R., Bleckmann, A. and Simon, R. (2008). The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934-946.
28. Ni, J. and Clark, S. E. (2006). Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol. 140, 726-733.
29. Nimchuk, Z. L., Tarr, P. T., Ohno, C., Qu, X. and Meyerowitz, E. M. (2011). Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr. Biol. 21, 345-352.
30. Ogawa, M., Shinohara, H., Sakagami, Y. and Matsubayashi, Y. (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294.
31. Ohyama, K., Shinohara, H., Ogawa-Ohnishi, M. and Matsubayashi, Y. (2009). A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 5, 578-580.
32. Prigge, M. J., Otsuga, D., Alonso, J. M., Ecker, J. R., Drews, G. N. and Clark, S. E. (2005). Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17, 61-76.
33. Rojo, E., Sharma, V. K., Kovaleva, V., Raikhel, N. V. and Fletcher, J. C. (2002). CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14, 969-977.
34. Schoof, H., Lenhard, M., Haecker, A., Mayer, K. F. X., Jürgens, G. and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635-644.
35. Sessions, A., Weigel, D. and Yanofsky, M. F. (1999). The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 20, 259-263.
36. Shinohara, H., Moriyama, Y., Ohyama, K. and Matsubayashi, Y. (2012). Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. Plant J. 70, 845-854.
37. Suzaki, T., Ohneda, M., Toriba, T., Yoshida, A. and Hirano, H.-Y. (2009). FON2 SPARE1 redundantly regulates floral meristem maintenance with FLORAL ORGAN NUMBER2 in rice. PLoS Genet. 5, e1000693.
38. Vieten, A., Vanneste, S., Wisńiewska, J., Benková, E., Benjamins, R., Beeckman, T., Luschnig, C. and Friml, J. (2005). Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132, 4521-4531.
39. Williams, L., Grigg, S. P., Xie, M., Christensen, S. and Fletcher, J. C. (2005). Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132, 3657-3668.
40. Yadav, R. K., Perales, M., Gruel, J., Ohno, C., Heisler, M., Girke, T., Jonsson, H. and Reddy, G. V. (2013). Plant stem cell maintenance involves direct transcriptional repression of differentiation program. Mol. Syst. Biol. 9, 654.
41. Yoshida, S., Mandel, T. and Kuhlemeier, C. (2011). Stem cell activation by light guides plant organogenesis. Genes Dev. 25, 1439-1450.
42. Zhao, C., Craig, J. C., Petzold, H. E., Dickerman, A. W. and Beers, E. P. (2005). The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol. 138, 803-818.