Weeds of change: Cardamine hirsuta as a new model system for studying dissected leaf development

Journal of Plant Research

Volumn 123, Issue 1, 2010, Pages 25-33

  Canales, Claudia ^a   Barkoulas, Michalis ^a   Galinha, Carla ^a   Tsiantis, Miltos ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Auxin; KNOX proteins; Leaf development

Indexed keywords

HOMEODOMAIN PROTEIN; PHYTOHORMONE;

CARDAMINE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; HOMEOBOX; INSULATOR ELEMENT; MERISTEM; PHYSIOLOGY; PLANT GENE; PLANT LEAF; REVIEW;

CARDAMINE; GENES, HOMEOBOX; GENES, PLANT; HOMEODOMAIN PROTEINS; INSULATOR ELEMENTS; MERISTEM; PLANT GROWTH REGULATORS; PLANT LEAVES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CARDAMINE; CARDAMINE HIRSUTA;

EID: 72249107316     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10265-009-0263-3     Document Type: Review

References (82)

1. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9: 841-857.
2. Aida M, Vernoux T, Furutani M, Traas J, Tasaka M (2002) Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129: 3965-3974.
3. Arber A (1950) The natural philosophy of plant form. Cambridge University Press, Cambridge.
4. Barkoulas M, Galinha C, Grigg SP, Tsiantis M (2007) From genes to shape: regulatory interactions in leaf development. Curr Opin Plant Biol 10: 660-666.
5. Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M (2008) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat Genet 40: 1136-1141.
6. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
7. Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N (2009) The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136: 823-832.
8. 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.
9. 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.
10. Brand A, Shirding N, Shleizer S, Ori N (2007) Meristem maintenance and compound-leaf patterning utilize common genetic mechanisms in tomato. Planta 246: 941-951.
11. 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.
12. Carroll SB (2005) Evolution at two levels: on genes and form. PLoS Biol 3: e245.
13. Champagne C, Sinha N (2004) Compound leaves: equal to the sum of their parts? Development 131: 4401-4412.
14. Claßen-Bockhoff R (2001) Plant morphology: the historic concepts of Wilheim Troll, Walter Zimmermann and Agnes Arber. Ann Bot (Lond) 88: 1153-1172.
15. Coen E, Rolland-Lagan AG, Matthews M, Bangham JA, Prusinkiewicz P (2004) The genetics of geometry. Proc Natl Acad Sci USA 101: 4728-4735.
16. Cretekos CJ, Wang Y, Green ED, Martin JF, Rasweiler JJt, Behringer RR (2008) Regulatory divergence modifies limb length between mammals. Genes Dev 22: 141-151.
17. De Smet I, Vanneste S, Inzé D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60: 871-887.
18. DeMason DA, Chawla R (2004) Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 218: 435-448.
19. Dengler NG, Tsukaya H (2001) Leaf morphogenesis in dicotyledons-current issues. Int J Plant Sci 162: 729-745.
20. Dolan L, Poethig RS (1998) Clonal analysis of leaf development in cotton. Am J Bot 85: 315-321.
21. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215: 407-419.
22. Dubrovsky JG, Rost TL, Colón-Carmona A, Doerner P (2001) Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214: 30-36.
23. Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105: 8790-8794.
24. Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20: 2293-2306.
25. Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M (2004) PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131: 5021-5030.
26. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226-2230.
27. Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433: 481-487.
28. Groot EP, Sinha N, Gleissberg S (2005) Expression patterns of STM-like KNOX and Histone H4 genes in shoot development of the dissected-leaved basal eudicot plants Chelidonium majus and Eschscholzia californica (Papaveraceae). Plant Mol Biol 58: 317-331.
29. Guo M, Thomas J, Collins G, Timmermans MC (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20: 48-58.
30. Hagemann W, Gleissberg S (1996) Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst Evol 199: 121-152.
31. Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E (1996) The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84: 735-744.
32. Hay A, Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsisthaliana and its wild relative Cardamine hirsuta. Nat Genet 38: 942-947.
33. Hay A, Barkoulas M, Tsiantis M (2004) PINning down the connections: transcription factors and hormones in leaf morphogenesis. Curr Opin Plant Biol 7: 575-581.
34. Hay A, Barkoulas M, Tsiantis M (2006) ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133: 3955-3961.
35. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15: 1899-1911.
36. Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M (2006) Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18: 2946-2957.
37. Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7: 581-587.
38. Jackson D, Veit B, Hake S (1994) Expression of maize KNOTTED-1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405-413.
39. Janssen BJ, Lund L, Sinha N (1998) Overexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf. Plant Physiol 117: 771-786.
40. 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. Curr Biol 15: 1560-1565.
41. Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, Carroll SB (2008) The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132: 783-793.
42. Kaplan DR (2001) Fundamental concepts of leaf morphology and morphogenesis: a contribution to the interpretation of molecular genetic mutants. Int J Plant Sci 162: 465-474.
43. Kenrick P, Crane PR (1997) The origin and early diversification of land plants: a cladistic study. Smithsonian Institution Press, London.
44. Koch M, Haubold B, Mitchell-Olds T (2001) Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am J Bot 88: 534-544.
45. Koenig D, Bayer E, Kang J, Kuhlemeier C, Sinha N (2009) Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136: 2997-3006.
46. Lacroix CR, Jeune B, Purcell-McDonald S (2003) Shoot and compound leaf comparisons in eudicots: dynamic morphology as an alternative approach. Bot J Linn Soc 143: 219-230.
47. Lawrence PA (2004) Last hideout of the unknown? Nature 429: 247.
48. Lihova J, Marhold K, Kudoh H, Koch MA (2006) Worldwide phylogeny and biogeography of Cardamine flexuosa (Brassicaceae) and its relatives. Am J Bot 93: 1206-1221.
49. 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.
50. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44.
51. Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126: 2979-2991.
52. McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG, Payre F, Stern DL (2007) Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448: 587-590.
53. Nath U, Crawford BC, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299: 1404-1407.
54. Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18: 2929-2945.
55. Nishimura A, Tamaoki M, Sato Y, Matsuoka M (1999) The expression of tobacco knotted1-type class 1 homeobox genes correspond to regions predicted by the cytohistological zonation model. Plant J 18: 337-347.
56. 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.
57. Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I, Alvarez JP, Blum E, Zamir D, Eshed Y (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39: 787-791.
58. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425: 257-263.
59. Poethig RS (1987) Clonal analysis of cell lineage patterns in plant development. Am J Bot 74: 581-594.
60. Poethig RS, Sussex IM (1985) The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165: 170-184.
61. Raff RA (2000) Evo-devo: the evolution of a new discipline. Nat Rev Genet 1: 74-79.
62. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426: 255-260.
63. Sattler R, Rutishauser R (1992) Partial homology of pinnate leaves and shoots: orientation of leaflet inception. Bot Jahrb Syst Pflanzengesh Planzengeogr 114: 61-79.
64. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20: 1015-1027.
65. Shani E, Yanai O, Ori N (2006) The role of hormones in shoot apical meristem function. Curr Opin Plant Biol 9: 484-489.
66. Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457: 818-823.
67. Sommer RJ (2009) The future of evo-devo: model systems and evolutionary theory. Nat Rev Genet 10: 416-422.
68. Steeves TA, Sussex IM (1989) Patterns in plant development. Cambridge University Press, Cambridge.
69. Stewart WN, Rothwell GW (1993) Paleobotany and the evolution of plants. Cambridge University Press, Cambridge.
70. Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128: 1127-1135.
71. Taylor S, Hofer J, Murfet I (2001) Stamina pistilloida, the Pea ortholog of Fim and UFO, is required for normal development of flowers, inflorescences, and leaves. Plant Cell 13: 31-46.
72. Timmermans MC, Hudson A, Becraft PW, Nelson T (1999) ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284: 151-153.
73. Tsiantis M, Schneeberger R, Golz JF, Freeling M, Langdale JA (1999) The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284: 154-156.
74. Uchida N, Townsley B, Chung K-H, Sinha N (2007) Regulation of SHOOTMERISTEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development. Proc Natl Acad Sci USA 104: 15953-15958.
75. Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10: 222-228.
76. Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127: 5157-5165.
77. Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC (2003) The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15: 1563-1577.
78. Wagner GP (2007) The developmental genetics of homology. Nat Rev Genet 8: 473-479.
79. 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.
80. Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latche A, Pech JC, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17: 2676-2692.
81. Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci USA 106: 4941-4946.
82. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15: 1566-1571.