Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches

New Phytologist

Volumn 199, Issue 4, 2013, Pages 1081-1092

  Nardmann, Judith ^a   Werr, Wolfgang ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Leaf development; Plant evolution; Stem cell niches; WOX phylogeny; WUSCHEL

Indexed keywords

COMMON ANCESTRY; GENE EXPRESSION; HISTOLOGY; LEAF MORPHOLOGY; PHYLOGENY; PLANT ARCHITECTURE; SEED; STEM;

EMBRYOPHYTA; GYMNOSPERMAE; MAGNOLIOPHYTA; SPERMATOPHYTA;

HOMEODOMAIN PROTEIN; VEGETABLE PROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; LEAF DEVELOPMENT; MERISTEM; METABOLISM; PHYLOGENY; PLANT EVOLUTION; PLANT LEAF; PLANT SEED; SEQUENCE HOMOLOGY; STEM CELL NICHE; STEM CELL NICHES; VASCULAR BUNDLE (PLANT); WOX PHYLOGENY; WUSCHEL;

LEAF DEVELOPMENT; PLANT EVOLUTION; STEM CELL NICHES; WOX PHYLOGENY; WUSCHEL;

GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; MERISTEM; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; PLANT VASCULAR BUNDLE; SEEDS; SEQUENCE HOMOLOGY, AMINO ACID; STEM CELL NICHE;

EID: 84881263928     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12343     Document Type: Article

References (59)

1. Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, Sinha NR. 2002. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296: 1858-1860.
2. Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P. 2008. A conserved molecular framework for compound leaf development. Science 322: 1835-1839.
3. Boyce CK. 2005. Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31: 117-149.
4. Boyce CK, Knoll AH. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28: 70-100.
5. Bradley D, Carpenter R, Sommer H, Hartley N, Coen E. 1993. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72: 85-95.
6. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. 2000. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289: 617-619.
7. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. 2008. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Developmental Cell 14: 867-876.
8. Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA. 2000. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408: 967-971.
9. Christenhusz MJM, Reveal JL, Farjon A, Gardner MF, Mill RR, Chase MA. 2011. A new classification and linear sequence of extant gymnosperms. Phytotaxa 19: 55-70.
10. Cibrian-Jaramillo A, De la Torre-Barcena JE, Lee EK, Katari MS, Little DP, Stevenson DW, Martienssen R, Coruzzi GM, DeSalle R. 2010. Using phylogenomic patterns and gene ontology to identify proteins of importance in plant evolution. Genome Biology and Evolution 2: 225-239.
11. Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, Moreau H, Kreis M, Lecharny A. 2008. Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evolutionary Biology 8: 291.
12. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG. 1999. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Developments in Biologicals 215: 407-419.
13. Fiume E, Fletcher JC. 2012. Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 24: 1000-1012.
14. Floyd SK, Bowman JL. 2010. Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology? Journal of Plant Research 123: 43-55.
15. Gifford EM, Foster AS. 1989. Morphology and evolution of vascular plants. New York, NY, USA: W.H. Freeman.
16. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T. 2004. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657-668.
17. Harrison CJ, Corley SB, Moylan EC, Alexander DL, Scotland RW, Langdale JA. 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434: 509-514.
18. Hirakawa Y, Kondo Y, Fukuda H. 2010. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22: 2618-2629.
19. Jackson D. 1991. In situ hybridization in plants. In: Bowles DJ, Gurr SJ, McPerson M, eds. Molecular plant pathology: a practical approach. Oxford, UK: Oxford University Press, 163-174.
20. Ji J, Shimizu R, Sinha N, Scanlon MJ. 2010a. Analyses of WOX4 transgenics provide further evidence for the evolution of the WOX gene family during the regulation of diverse stem cell functions. Plant Signaling and Behavior 5: 916-920.
21. Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ. 2010b. WOX4 promotes procambial development. Plant Physiology 152: 1346-1356.
22. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
23. Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M. 2003. Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant Journal 35: 429-441.
24. Kenrick P, Crane PR. 1997. The origin and early evolution of plants on land. Nature 389: 33-39.
25. Lee EK, Cibrian-Jaramillo A, Kolokotronis SO, Katari MS, Stamatakis A, Ott M, Chiu JC, Little DP, Stevenson DW, McCombie WR et al. 2011. A functional phylogenomic view of the seed plants. PLoS Genetics 7: e1002411.
26. Matsumoto N, Okada K. 2001. A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes & Development 15: 3355-3364.
27. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805-815.
28. Muller R, Bleckmann A, Simon R. 2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20: 934-946.
29. Mundry M, Stützel T. 2004. Morphogenesis of leaves and cones of male short-shoots of Ginkgo biloba L. Flora 199: 437-452.
30. Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K. 2012. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24: 519-535.
31. Nardmann J, Ji J, Werr W, Scanlon MJ. 2004. The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131: 2827-2839.
32. Nardmann J, Reisewitz P, Werr W. 2009. Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Molecular Biology and Evolution 26: 1745-1755.
33. Nardmann J, Werr W. 2006. The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Molecular Biology and Evolution 23: 2492-2504.
34. Nardmann J, Werr W. 2012. The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns. Plant Molecular Biology 78: 123-134.
35. Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W. 2007. WOX gene phylogeny in Poaceae: a comparative approach addressing leaf and embryo development. Molecular Biology and Evolution 24: 2474-2484.
36. Ohmori Y, Tanaka W, Kojima M, Sakakibara H, Hirano HY. 2013. WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice. Plant Cell 25: 229-241.
37. Piazza P, Bailey CD, Cartolano M, Krieger J, Cao J, Ossowski S, Schneeberger K, He F, de Meaux J, Hall N et al. 2010. Arabidopsis thaliana leaf form evolved via loss of KNOX expression in leaves in association with a selective sweep. Current Biology 20: 2223-2228.
38. Sacher JA. 1955a. Cataphyll ontogeny in Pinus lambertiana. American Journal of Botany 42: 82-91.
39. Sacher JA. 1955b. Dwarf shoot ontogeny in Pinus lambertiana. American Journal of Botany 42: 784-792.
40. Sanders HL, Darrah PR, Langdale JA. 2011. Sector analysis and predictive modelling reveal iterative shoot-like development in fern fronds. Development 138: 2925-2934.
41. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T. 2007. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814.
42. Scanlon MJ. 2000. NARROW SHEATH1 functions from two meristematic foci during founder-cell recruitment in maize leaf development. Development 127: 4573-4585.
43. Scanlon MJ, Schneeberger RG, Freeling M. 1996. The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 122: 1683-1691.
44. Schneeberger R, Tsiantis M, Freeling M, Langdale JA. 1998. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125: 2857-2865.
45. Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens 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.
46. Shimizu R, Ji J, Kelsey E, Ohtsu K, Schnable PS, Scanlon MJ. 2009. Tissue specificity and evolution of meristematic WOX3 function. Plant Physiology 149: 841-850.
47. Stahl Y, Wink RH, Ingram GC, Simon R. 2009. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Current Biology 19: 909-914.
48. Suer S, Agusti J, Sanchez P, Schwarz M, Greb T. 2011. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23: 3247-3259.
49. Sussex IM. 1989. Developmental programming of the shoot meristem. Cell 56: 225-229.
50. Tadege M, Lin H, Bedair M, Berbel A, Wen J, Rojas CM, Niu L, Tang Y, Sumner L, Ratet P et al. 2011. STENOFOLIA regulates blade outgrowth and leaf vascular patterning in Medicago truncatula and Nicotiana sylvestris. Plant Cell 23: 2125-2142.
51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
52. Tomescu AM. 2009. Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science 14: 5-12.
53. Tomlinson PB, Fisher JB. 2005. Development of nonlignified fibers in leaves of Gnetum gnemon (Gnetales). American Journal of Botany 92: 383-389.
54. Trotochaud AE, Hao T, Wu G, Yang Z, Clark SE. 1999. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11: 393-406.
55. Tsukaya H. 2002. Leaf development. Arabidopsis Book 1: e0072.
56. Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS, Gerats T. 2009. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell 21: 2269-2283.
57. Waites R, Selvadurai HR, Oliver IR, Hudson A. 1998. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93: 779-789.
58. Yadav RK, Perales M, Gruel J, Girke T, Jonsson H, Reddy GV. 2011. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes & Development 25: 2025-2030.
59. Zhong B, Deusch O, Goremykin VV, Penny D, Biggs PJ, Atherton RA, Nikiforova SV, Lockhart PJ. 2011. Systematic error in seed plant phylogenomics. Genome Biology and Evolution 3: 1340-1348.