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

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Abstract

Cardamine hirsuta, a small crucifer closely related to the model organism Arabidopsis thaliana, offers high genetic tractability and has emerged as a powerful system for studying the genetic basis for diversification of plant form. Contrary to A. thaliana, which has simple leaves, C. hirsuta produces dissected leaves divided into individual units called leaflets. Leaflet formation requires activity of Class I KNOTTED1-like homeodomain (KNOX) proteins, which also promote function of the shoot apical meristem (SAM). In C. hirsuta, KNOX genes are expressed in the leaves whereas in A. thaliana their expression is confined to the SAM, and differences in expression arise through cis-regulatory divergence of KNOX regulation. KNOX activity in C. hirsuta leaves delays the transition from proliferative growth to differentiation thus facilitating the generation of lateral growth axes that give rise to leaflets. These axes reflect the sequential generation of cell division foci across the leaf proximodistal axis in response to auxin activity maxima, which are generated by the PINFORMED1 (PIN1) auxin efflux carriers in a process that resembles organogenesis at the SAM. Delimitation of C. hirsuta leaflets also requires the activity of CUP SHAPED COTYLEDON (CUC) genes, which direct formation of organ boundaries at the SAM. These observations show how species-specific deployment of fundamental shoot development networks may have sculpted simple versus dissected leaf forms. These studies also illustrate how extending developmental genetic studies to morphologically divergent relatives of model organisms can greatly help elucidate the mechanisms underlying the evolution of form.

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References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Arber A (1950) The natural philosophy of plant form. Cambridge University Press, Cambridge

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Carroll SB (2005) Evolution at two levels: on genes and form. PLoS Biol 3:e245

    Article  PubMed  CAS  Google Scholar 

  • Champagne C, Sinha N (2004) Compound leaves: equal to the sum of their parts? Development 131:4401–4412

    Article  PubMed  CAS  Google Scholar 

  • Claßen-Bockhoff R (2001) Plant morphology: the historic concepts of Wilheim Troll, Walter Zimmermann and Agnes Arber. Ann Bot (Lond) 88:1153–1172

    Article  Google Scholar 

  • Coen E, Rolland-Lagan AG, Matthews M, Bangham JA, Prusinkiewicz P (2004) The genetics of geometry. Proc Natl Acad Sci USA 101:4728–4735

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • DeMason DA, Chawla R (2004) Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 218:435–448

    Article  PubMed  CAS  Google Scholar 

  • Dengler NG, Tsukaya H (2001) Leaf morphogenesis in dicotyledons—current issues. Int J Plant Sci 162:729–745

    Article  Google Scholar 

  • Dolan L, Poethig RS (1998) Clonal analysis of leaf development in cotton. Am J Bot 85:315–321

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Rost TL, Colón-Carmona A, Doerner P (2001) Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214:30–36

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20:2293–2306

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hagemann W, Gleissberg S (1996) Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst Evol 199:121–152

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hay A, Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38:942–947

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kenrick P, Crane PR (1997) The origin and early diversification of land plants: a cladistic study. Smithsonian Institution Press, London

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Koenig D, Bayer E, Kang J, Kuhlemeier C, Sinha N (2009) Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136:2997–3006

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lawrence PA (2004) Last hideout of the unknown? Nature 429:247

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    PubMed  CAS  Google Scholar 

  • Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–2991

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nath U, Crawford BC, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Poethig RS (1987) Clonal analysis of cell lineage patterns in plant development. Am J Bot 74:581–594

    Article  Google Scholar 

  • Poethig RS, Sussex IM (1985) The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165:170–184

    Article  Google Scholar 

  • Raff RA (2000) Evo-devo: the evolution of a new discipline. Nat Rev Genet 1:74–79

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sattler R, Rutishauser R (1992) Partial homology of pinnate leaves and shoots: orientation of leaflet inception. Bot Jahrb Syst Pflanzengesh Planzengeogr 114:61–79

    Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027

    Article  PubMed  CAS  Google Scholar 

  • Shani E, Yanai O, Ori N (2006) The role of hormones in shoot apical meristem function. Curr Opin Plant Biol 9:484–489

    Article  PubMed  CAS  Google Scholar 

  • Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457:818–823

    Article  PubMed  CAS  Google Scholar 

  • Sommer RJ (2009) The future of evo-devo: model systems and evolutionary theory. Nat Rev Genet 10:416–422

    PubMed  CAS  Google Scholar 

  • Steeves TA, Sussex IM (1989) Patterns in plant development. Cambridge University Press, Cambridge

    Google Scholar 

  • Stewart WN, Rothwell GW (1993) Paleobotany and the evolution of plants. Cambridge University Press, Cambridge

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Uchida N, Townsley B, Chung K-H, Sinha N (2007) Regulation of SHOOT MERISTEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development. Proc Natl Acad Sci USA 104:15953–15958

    Article  PubMed  Google Scholar 

  • Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10:222–228

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wagner GP (2007) The developmental genetics of homology. Nat Rev Genet 8:473–479

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) BB/F012934/1 and the Gatsby Foundation. We thank J. Baker for photography. M.T. is a recipient of an EMBO Young Investigator Award and a Royal Society Wolfson Merit award.

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  1. Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK

    Claudia Canales, Michalis Barkoulas, Carla Galinha & Miltos Tsiantis

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  1. Claudia Canales
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Canales, C., Barkoulas, M., Galinha, C. et al. Weeds of change: Cardamine hirsuta as a new model system for studying dissected leaf development. J Plant Res 123, 25–33 (2010). https://doi.org/10.1007/s10265-009-0263-3

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