Skip to main content
SpringerLink
Log in

Parallelismic homoplasy of leaf and stipule phenotypes among genetic variants of Pisum sativum and Medicago truncatula and some taxa of Papilionoideae, Caesalpinioideae and Mimosoideae subfamilies of the Leguminosae flora of Delhi

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The leguminous flora of Delhi comprises 78 Papilionoideae, 24 Caesalpinioideae and 24 Mimosoideae species; 80 of them are perennials. Five types of imparipinnate and two types of paripinnate compound leaves were observed in the species. The paripinnate leaves are bipinnate in 25 species (mostly mimosoid) and bifoliate in two species. The imparipinnate leaves were trifoliate or multifoliate in 59 papilionoid species and multifoliate in 16 caesalpinioid species; four of the papilionoid species produced leafletted and tendrilled unipinnate leaves. Leaves were bifacially simple in 22 species, simple with ectopic terminal growth in one species and simple tendril in one species. Twenty-one species (mostly mimosoid) were devoid of stipules. In 82 species stipules were small and free. Stipules were large and lobed in 17 species and large and adnate in four species. Two species of Caesalpinioideae produce compound leaf-like stipules. All four stipule phenotypes of 126 species corresponded with stipular phenotypes observed in wild type, coch, st and coch st genotypes of the model legume P. sativum. The seven leaf phenotypes observed in 126 species corresponded with phenotypes expected among combinations of uni (uni-tac), af, ins, mfp and tl mutants of P. sativum and sgl1, cfl1, slm1 and palm1 mutants of M. truncatula, also an IRL model legume. All the variation in leaf and stipule morphologies observed in the leguminous flora of Delhi could be explained in terms of the gene regulatory networks already revealed in P. sativum and M. truncatula. It is hypothesized that the ancestral gene regulatory networks for leaves and stipules produced in Leguminosae were like that prevalent in P. sativum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Aida M, Tasaka M (2006) Genetic control of shoot organ boundaries. Curr Opin Plant Biol 9:72–77

    Article  PubMed  CAS  Google Scholar 

  • Bell AD, Bryan A (2008) Plant form: an illustrated guide to flowering plant morphology. Timber Press, Portland, pp 78–79

    Google Scholar 

  • Belles-Boix E, Hamant O, Witiak SM, Morin H, Traas J, Pautot V (2006) KNAT6: an Arabidopsis homeobox gene involved in meristem activity and organ separation. Plant Cell 18:1900–1907

    Article  PubMed  CAS  Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Scifertova D, Jurgens G, Firm J (2003) Local, efflux dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  CAS  Google Scholar 

  • Bews JW (1922) The South-East African flora: its origin, migrations and evolutionary tendencies. Ann Bot Lond 36:209–223

    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 

  • Blixt S (1967) Linkage studies in Pisum VII. The manifestation of the genes cri and coch, and the double-recessive in Pisum. Agri Hortique Genetica 25:131–144

    Google Scholar 

  • Blixt S (1972) Mutation genetics in Pisum. Agri Hortique Genetica 30:1–293

    Google Scholar 

  • Braybrook S, Kuhlemeier C (2010) How a plant builds leaves. Plant Cell 22:1006–1018

    Article  PubMed  CAS  Google Scholar 

  • Champagne CEM, Goliber TE, Wojciechowski MP, Townsley BT, Wang K, Paz MM, Geeta R, Sinha NR (2007) Compound leaf development and evolution in the legumes. Plant Cell 19:3369–3378

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Yub J, Gea L, Wang H, Berbel A, Liu Y, Chen Y, Li G, Tadegea M, Wen J, Cosson V, Mysorea KS, Ratetd P, Madueñoc F, Bai G, Chen R (2010) Control of dissected leaf morphology by a Cys(2)His(2) inc finger transcription factor in the model legume Medicago truncatula. Proc Natl Acad Sci USA 107:10754–10759

    Article  PubMed  CAS  Google Scholar 

  • Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554

    Article  PubMed  CAS  Google Scholar 

  • Cote R, Gerrath JM, Posluszny U, Grodzinski B (1992) Comparative leaf development of conventional and semileafless peas (Pisum sativum). Can J Bot 70:571–580

    Article  Google Scholar 

  • Cracraft J (2005) Phylogeny and evo-devo characters, homology and the historical analysis of the evolution of development. Zoology 108:345–356

    Article  PubMed  Google Scholar 

  • Cronk Q, Ojeda I, Pennington RT (2006) Legume comparative genomics: progress in phylogenetics and phylogenomics. Curr Opin Plant Biol 9:99–103

    Article  PubMed  CAS  Google Scholar 

  • Cronquist A (1988) The evolution and classification of flowering plants. NY Bot Garden Press, NY 556

    Google Scholar 

  • de Vilmorin P, Bateson W (1911) A case of gametic coupling in Pisum. Proc R Soc Lond Ser B Biol Sci 84:9–11

    Article  Google Scholar 

  • DeMason DA (2005) Extending Marx’s isogenic lines in search of Uni function. Pisum Genetics 37:10–14

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • DeMason DA, Schmidt RJ (2001) Roles of the uni gene in shoot and leaf development of pea (Pisum sativum): phenotypic characterization and leaf development in the uni and uni-tac mutants. Int J Plant Sci 162:1033–1051

    Article  CAS  Google Scholar 

  • DeMason DA, Villani PJ (2001) Genetic control of leaf development in pea (Pisum sativum). Int J Plant Sci 162:493–511

    Article  CAS  Google Scholar 

  • Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 131:900–910

    Article  PubMed  CAS  Google Scholar 

  • Eames AJ (1961) Morphology of the angiosperms. McGraw-Hill, New York, pp 518

  • Emery JF, Floyd SK, Alvarej J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-zip and KANAD1 genes. Curr Biol 13:1768–1774

    Article  PubMed  CAS  Google Scholar 

  • Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997–3006

    Article  PubMed  CAS  Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944

    Article  PubMed  CAS  Google Scholar 

  • Fawole I (2001) Genetic analysis of mutations at loci controlling leaf form in Cowpea (Vigna unguiculata [L] Walp.). J Hered 92:43–50

    Article  PubMed  CAS  Google Scholar 

  • Ferrandiz C, Navarro C, Gomez MD, Canas LA, Beltran JP (1999) Flower development in Pisum sativum: from the war of the whorls to the battle of common primordia. Dev Genet 25:280–290

    Article  PubMed  Google Scholar 

  • Finet C, Fourquin C, Vinauger M, Berne-Dedieu A, Chambrier P, Paindavoine S, Scutt CP (2010) Parallel Structural evolution of auxin response factors in angiosperms. Plant J 63:952–959

    Article  PubMed  CAS  Google Scholar 

  • Floyd SK, Bowman JL (2010) Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology? J Plant Res 123:43–55

    Article  PubMed  CAS  Google Scholar 

  • Geeta R, Davalos LM, Levy A, Bohs L, Lavin M, Mumenhoff K, Sinha N, Wojciechowski MF (2012) Keeping it simple: flowering plants tend to retain and revert to simple leaves. New Phytol 193:481–493

    Article  PubMed  CAS  Google Scholar 

  • Gepts P, Beavis WD, Brummer EC, Shoemaker RC, Stalker HT, Weeden NF, Young ND (2005) Legumes as a model plant family. Genomics for food and feed report of the cross-legume advances through genomics conference. Plant Physiol 137:1228–1235

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg JB (1965) Afila, a new mutant in pea (Pisum sativum L.). Boletin Genetico 1:27–31

    Google Scholar 

  • Gould KS, Cutter EG, Young JPW (1986) Morphogenesis of the compound leaf in three genotypes of the pea, Pisum sativum. Can J Bot 64:1268–1276

    Article  Google Scholar 

  • Gourlay CW, Hofer JMI, Ellis THN (2000) Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, COCHLEATA, AFILA and TENDRILLESS. Plant Cell 12:1279–1294

    PubMed  CAS  Google Scholar 

  • Hake S, Smith HMS, Holtan H, Magnani E, Mele G, Ramirej J (2004) The role of KNOX genes in plant development. Annu Rev Cell Dev Biol 20:125–151

    Article  PubMed  CAS  Google Scholar 

  • Hofer JM, Turner I, Hellens R, Ambrose M, Mathews P, Michael A, Ellis TH (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7:581–587

    Article  PubMed  CAS  Google Scholar 

  • Hofer J, Gourlay C, Michael A, Ellis THN (2001) Expression of a class I knotted-1 like homeobox gene is down-regulated in pea compound leaf primordia. Plant Mol Biol 45:387–391

    Article  PubMed  CAS  Google Scholar 

  • Hofer JM, Turner I, Moreau C, Ambrose M, Isaac P, Butcher S, Weller J, Dupin A, Dalmais M, Le Signor C, Bendahmane A, Ellis TH (2009) Tendril-less regulates tendril formation in pea leaves. Plant Cell 21:420–428

    Article  PubMed  CAS  Google Scholar 

  • Hooker WJ (1821) Flora Scotica: or a description of Scottish plants. William Jackson Hooker, London, pp 307

  • Hooker JH (1875) Flora of British India, vol 1–6. London L Reeve, London

  • Hornstein E, Shomoron N (2006) Canalization of development by microRNAs. Nat Genet 38:S20–S24

    Article  PubMed  CAS  Google Scholar 

  • Hunter C, Wilman MR, Wu G, Yoshikwa M, de la Luz Gutierrez-Nava M, Poethig SR (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulate heteroblasty in Arabidopsis. Development 133:2973–2981

    Article  PubMed  CAS  Google Scholar 

  • Husbands AY, Chitwood DH, Plavskin Y, Timmermans MCP (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997

    Article  PubMed  CAS  Google Scholar 

  • Kinder CA (2010) The many roles of small RNAs in leaf development. J Genet Genomics 37:13–21

    Article  CAS  Google Scholar 

  • Kubitzki K, von Sengbusch P, Poppendieck H–H (1991) Parallelism, its evolutionary origin and systematic significance. Aliso 13:191–206

    Google Scholar 

  • Kumar S and Sharma V (2012) Abnormal leaf morphologies associated with primary and secondary vein patterning defects in Catharanthus roseus: mid-vein defect converts simple leaf into binate compound leaf. Proc Natl Acad Sci, India Sect B Biol Sci doi: 10.1007/s40011-012-0090-5

  • Kumar S, Rai SK, Pandey-Rai S, Srivastava S, Singh D (2004) Regulation of unipinnate character in the distal tendrilled domain of compound leaf-blade by the gene MULTIFOLIATE PINNA (MFP) in pea Pisum sativum. Plant Sci 166:929–940

    Article  CAS  Google Scholar 

  • Kumar S, Mishra RK, Chaudhary S, Pandey R, Yadav G (2009a) Co-regulation of biomass partitioning by leafblade morphology genes AFILA, MULTIFOLIATE-PINNA, TENDRIL-LESS and UNIFOLIATA in grain pea Pisum sativum. Proc Ind Nat Sci Acad 75:15–26

    CAS  Google Scholar 

  • Kumar S, Mishra RK, Kumar A, Srivastava S, Chaudhary S (2009b) Regulation of stipule development by COCHLEATA and STIPULE- REDUCED genes in pea (Pisum sativum). Planta 230:449–458

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Chaudhary S, Sharma V, Kumari R, Mishra RK, Kumar A, Choudhury DR, Jha R, Priyadarshini A, Kumar A (2010) Genetic control of leaf-blade morphogenesis by the INSECATUS gene in Pisum sativum. J Genet 89:201–211

    Article  PubMed  Google Scholar 

  • Kumar S, Sharma V, Chaudhary S, Kumari R, Kumari N, Mishra P (2011) Interaction between COCHLEATA and UNIFOLIATA genes enables a normal flower morphogenesis in the garden pea Pisum sativum. J Genet 90:309–314

    Article  PubMed  Google Scholar 

  • Kumar A, Sharma V, Khan M, Hindala M, Kumar S (2012a) Auxin transport inhibitor induced low complexity petiolated leaves and sessile leaflike stipules and architectures of heritable leaf and stipule mutants in Pisum sativum suggest that its simple lobed stipules and compound leaf represent ancestral forms in angiosperms. J Genet (in press)

  • Kumar A, Sharma V, Khan M, Tripathi BN and Kumar S (2012b) Pisum sativum wild-type and mutant stipules and those induced by an auxin transport inhibitor demonstrate the entire diversity of laminated stipules observed in angiosperms. Protoplasma (Published online) doi:10.1007/s00709-012-0397-3

  • Lamprecht H (1933) Ein unifoliata Typus von Pisum mit gleichzeitiger Pistilloidie. Hereditas 18:56–64

    Article  Google Scholar 

  • Lamprecht H (1959) Das Merkmal insecatus von Pisum und seine Vererbung sowie einige Koppelungsstudien. Agri Hortique Genetica 17:26–36

    Google Scholar 

  • Laufs P, Peaucelle A, Morin H, Trass J (2004) Micro RNA regulation of CUC genes is required for boundary size control in Arabidopsis meristem. Development 131:4311–4322

    Article  PubMed  CAS  Google Scholar 

  • Lewis G, Schrire B (2002) Legumes of the World. Royal Bot Gardens, Kew, p 592

  • Lewis G, Schrire B, Mackinder B, Lock M (2005) Legumes of the World. Royal Bot Garden, Kew Publishing, Kew, p 592

    Google Scholar 

  • Lu B, Villani PJ, Watson JC, DeMason DA, Cooke TJ (1996) The control of pinna morphology in wildtype and mutant leaves of the garden pea (Pisum sativum L). Int J Plant Sci 157:659–673

    Article  Google Scholar 

  • Lubbock J (1891) On stipules, their form and function. J Linn Soc Bot 28:217–243

    Article  Google Scholar 

  • Maheshwari JK (1963) The flora of Delhi. Council of Scientific and Industrial Research, New Delhi, p 447

    Google Scholar 

  • Marx GA (1987) A suit of mutants that modify pattern formation in pea leaves. Plant Mol Biol Rep 5:311–335

    Article  Google Scholar 

  • McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    Article  PubMed  CAS  Google Scholar 

  • McHale NA, Koning RF (2004) PHANTASTICA regulates development of the adaxial mesophyll in Nicotiana leaves. Plant Cell 16:1251–1262

    Article  PubMed  CAS  Google Scholar 

  • Meicenheimer RD, Muchlbauer FJ, Hindman JL, Gritton ET (1983) Meristem characteristics of genetically modified pea (Pisum sativum) leaf primordia. Can J Bot 61:3430–3437

    Article  Google Scholar 

  • Mishra RK, Chaudhary S, Kumar A, Kumar S (2009) Effects of MULTIFOLIATE-PINNA, AFILA, TENDRIL-LESS and UNIFOLIATA genes on leaf blade architecture in Pisum sativum. Planta 230:177–190

    Article  PubMed  CAS  Google Scholar 

  • Monti LM, Devreux M (1969) Stamina pistilloida: a new mutation induced in pea. Theor Appl Genet 39:17–20

    Article  Google Scholar 

  • Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Func Plant Biol 38:535–552

    Article  Google Scholar 

  • Nogueira FT, Madi S, Chitwood DM, Juarez MT, Timmermans MC (2007) Two small regulatory RNAs establishing opposing fates of a development axis. Genes Dev 21:750–755

    Article  PubMed  CAS  Google Scholar 

  • Pekker I, Alvarej JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910

    Article  PubMed  CAS  Google Scholar 

  • Pellew C, Sverdrup A (1923) New observations on the genetics of peas (Pisum sativum). J Genet 13:125–131

    Article  Google Scholar 

  • Peng J, Rujin Chen R (2011) Auxin efflux transporter MtPIN10 regulates compound leaf and flower development in Medicago truncatula. Plant Signal Behav 6:1537–1544

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Yu J, Wang H, Guo Y, Li G, Bai S, Chen R (2011) Regulation of Compound Leaf Development in Medicago truncatula by Fused Compound Leaf1, a Class M KNOX Gene. Plant cell 23:3929–3943

    Article  PubMed  CAS  Google Scholar 

  • Prajapati S, Kumar S (2002) Interaction of the UNIFOLIATA TENDRILLED ACACIA gene with AFILA and TENDRIL-LESS genes in the determination of leaf blade growth and morphology in pea Pisum sativum. Plant Sci 162:713–721

    Article  CAS  Google Scholar 

  • Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76

    Article  PubMed  CAS  Google Scholar 

  • Rohlf JF (2000) NTSYSpc: Numerical Taxonomy and Multivariate Analysis System, Version 2.1, Exeter Software, Setauket, New York

  • Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi P, Turner J, Muday G, Estelle M (1997) Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar transport and diverse morphological defects. Plant Cell 9:745–757

    PubMed  CAS  Google Scholar 

  • Rutishauser R, Grob V, Pfeifer E (2008) Plants are used to having identity crises. In: Minelli A, Fusco G (eds) Key themes in evolutionary developmental biology. Cambridge University Press, Cambridge, pp 194–213

    Chapter  Google Scholar 

  • Sambamurty AVSS (2005) Taxonomy of angiosperms. IK International Pvt Ltd, New Delhi, pp 299–332

    Google Scholar 

  • Sarojam R, Sappl PG, Goldscmidt A, Efroni I, Floyd SK, Eshed Y, Bowman JL (2010) Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell 22:2113–2130

    Article  PubMed  CAS  Google Scholar 

  • Scotland RW (2010) Deep homology: a view from systematic. BioEssays 32:438–449

    Article  PubMed  Google Scholar 

  • Scotland RW (2011) What is parallelism? Evo Devl 13:214–227

    Article  Google Scholar 

  • Sharma B, Kumar S (1981) Discovery of one more allele of the tac-locus of Pisum sativum. Pulse Crops Newsletter 4:50

    Google Scholar 

  • Sharma V, Kumar S (2012) Stipules are the Principal Photosynthetic Organs in the Papilionoid Species Lathyrus aphaca. Nat Acad Sci Lett 35:75–78. doi:10.1007/s40009-012-0031-0

    Article  Google Scholar 

  • Sharma V, Chaudhary S, Kumar A, Kumar S (2012a) COCHLEATA controls leaf size and secondary inflorescence architecture via negative regulation of UNIFOLIATA (LEAFY ortholog) gene in garden pea Pisum sativum. J Biosci 37:1–19. doi:10.1007/s12038-012-9263-x

    Article  CAS  Google Scholar 

  • Sharma V, Sinha AK, Chaudhary S, Priyadarshini A, Tripathi BN, Kumar S (2012b) Genetic analysis of structure and function of stipules in pea Pisum sativum. Proc Ind Nat Sci Acad 78:9–34

    Google Scholar 

  • Sharma V, Tripathi BN, Kumar S (2012c) Organ-wise homologies of stipule, leaf and inflorescence between Pisum sativum genetic variants, Delonix regia and Caesalpinia bonduc indicate parallel evolution of morphogenetic regulation. Plant Syst Evol 298:1167–1176

    Article  Google Scholar 

  • Smirnova OG (2002) Characteristics and inheritance of the leaf mutation ins. Pisum Genet 34:34–35

    Google Scholar 

  • Tattersall AD, Turner L, Knox MR, Ambrose MJ, Ellis THN, Hofer JMI (2005) The mutant crispa reveals multiple roles for PHANTASTICA in pea compound leaf development. Plant Cell 17:1046–1060

    Article  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

    PubMed  CAS  Google Scholar 

  • Townsley BT, Sinha NR (2012) A new development: evolving concepts in leaf ontogeny. Ann Rev Plant Biol 63:535–562

    Article  CAS  Google Scholar 

  • Tsukaya H (2010) Leaf development and evolution. J Plant Res 123:3–6

    Article  PubMed  Google Scholar 

  • Tyler AA (1897) The nature and origin of stipules. Ann NY Acad Sci 10:1–49

    Article  Google Scholar 

  • Uchida N, Kumar S, Koenig D, Sinha N (2010) Coordination of leaf development via regulation of KNOX1 genes. J Plant Res 123:7–14

    Article  PubMed  CAS  Google Scholar 

  • Van Steenis, de Wilde (1989) Flora Malesiana, vol 10, Kluwer Academic, USA, pp 668

  • Vavilov NI (1922) The law of homologous series in variation. J Genet 12:47–89

    Article  Google Scholar 

  • Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) PINFORMED 1 regulates cell fates at the periphery of the shoot apical meristem. Development 120:5157–5165

    Google Scholar 

  • Villani PJ, DeMason DA (1997) Roles of the AF and TL genes in pea leaf morphogenesis: characterization of the double mutant (af af tl tl). Am J Bot 84:1323–1336

    Article  PubMed  CAS  Google Scholar 

  • Vroemen CW (2003) The CUP-SHAPED COTYLEDON 3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15:1563–1577

    Article  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 

  • Wake DB, Wake MH, Specht CD (2011) Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331:1032–1035

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Chen J, Wen J, Tadege M, Li G, Liu Y, Mysore KS, Ratet P, Chen R (2008) Control of Compound Leaf Development by FLORICAULA/LEAFY Ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol 146:1759–1772

    Article  PubMed  CAS  Google Scholar 

  • White OE (1917) Studies of inheritance in Pisum II: the present state of knowledge of heredity and variation in peas. Proc Am Philos Soc 56:487–588

    Google Scholar 

  • Wojciechouski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matk gene resolves many well supported with in the family. Am J Bot 91:1846–1862

    Article  Google Scholar 

  • Wu G, Lin WC, Huang T, Poethig RS, Springer PS, Kerstetter RA (2008) KANADI 1 regulates adaxial-abaxial polarity in Arabidopsis by directly repressing the transcription of ASYMMETRIC LEAVES 2. Proc Natl Acad Sci USA 105:16392–16397

    Article  PubMed  CAS  Google Scholar 

  • Yamada T, Yokota S, Hirayama Y, Imaichi R, Kato M, Gasser CS (2011) Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms. Plant J 67:26–36

    Article  PubMed  CAS  Google Scholar 

  • Yap IV, Nelson RJ (1996) Winboot: a program for performing bootstrap analysis of binary data to determine the confidence limits of UPGMA-based dendrograms. IRRI 11(1):5461 discussion paper, pp 14.22

    Google Scholar 

  • Yaxley JL, Jablonski W, Reid JB (2001) Leaf and flower development in pea (Pisum sativum L.): mutants cochleata and unifoliata. Ann Bot 88:225–234

    Article  CAS  Google Scholar 

  • Yoon H-S, Baum DA (2004) Transgenic study of parallelism in plant morphological evolution. Proc Natl Acad Sci USA 101:6524–6529

    Article  PubMed  CAS  Google Scholar 

  • Zhou GK, Kubo M, Zhong R, Demura T, Ye ZH (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48:391–404

    Article  PubMed  CAS  Google Scholar 

  • Zhou C, Han L, Hou C, Metelli A, Qi L, Tadege M, Mysore KS, Wang ZY (2011) Developmental analysis of a Medicago truncatula smooth leaf margin1 mutant reveals context-dependent effects on compound leaf development. Plant Cell 23:2106–2124

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Grateful thanks are due to the Indian National Science Academy for a scientistship to SK, to the Director of the institute for facilities, to SKA Institution for Research, Education and Development for a postgraduate fellowship to VS and to the curators of the herbaria at the Botany Department of Delhi University and National Botanical Research Institute at Lucknow for allowing us to observe plant specimens. We also wish to thank F. James Rohlf for providing us a complimentary copy of the NTSYSpc 2.11x and highly useful discussion via email.

Author information

Authors and Affiliations

  1. National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, 110067, New Delhi, India

    Vishakha Sharma & Sushil Kumar

  2. SKA Institution for Research, Education and Development (SKAIRED), 4/11 Sarv Priya Vihar, 110016, New Delhi, India

    Vishakha Sharma & Sushil Kumar

Authors
  1. Vishakha Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sushil Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sushil Kumar.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 44 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharma, V., Kumar, S. Parallelismic homoplasy of leaf and stipule phenotypes among genetic variants of Pisum sativum and Medicago truncatula and some taxa of Papilionoideae, Caesalpinioideae and Mimosoideae subfamilies of the Leguminosae flora of Delhi. Plant Syst Evol 299, 887–911 (2013). https://doi.org/10.1007/s00606-013-0771-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-013-0771-4

Keywords

Search

Navigation