Abstract
UNIFOLIATA [(UNI) or UNIFOLIATA-TENDRILLED ACACIA (UNI-TAC)] expression is known to be negatively regulated by COCHLEATA (COCH) in the differentiating stipules and flowers of Pisum sativum. In this study, additional roles of UNI and COCH in P. sativum were investigated. Comparative phenotyping revealed pleiotropic differences between COCH (UNI-TAC and uni-tac) and coch (UNI-TAC and uni-tac) genotypes of common genetic background. Secondary inflorescences were bracteole-less and bracteolated in COCH and coch genotypes, respectively. In comparison to the leaves and corresponding sub-organs and tissues produced on COCH plants, coch plants produced leaves of 1.5-fold higher biomass, 1.5-fold broader petioles and leaflets that were 1.8-fold larger in span and 1.2-fold dorso-ventrally thicker. coch leaflets possessed epidermal cells 1.3-fold larger in number and size, 1.4-fold larger spongy parenchyma cells and primary vascular bundles with 1.2-fold larger diameter . The transcript levels of UNI were at least 2-fold higher in coch leaves and secondary inflorescences than the corresponding COCH organs. It was concluded that COCH negatively regulated UNI in the differentiating leaves and secondary inflorescences and thereby controlled their sizes and/or structures. It was also surmised that COCH and UNI (LFY homolog) occur together widely in stipulate flowering plants.
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Alvarez J, Guli CL, Yu X-H, et al. 1992 Terminal flower: A gene affecting inflorescence development in Arabidopsis thaliana. Plant J. 2 103–110
Bell AD and Bryan A 2008 Plant form: An illustrated guide to flowering plant morphology (Timber Press) pp 78–79
Benlloch R, Berbel A, Serrano-Mislata A, et al. 2007 Floral initiation and inflorescence architecture: a comparative view. Ann. Bot. 100 659–676
Blazquez MA, Ferrandiz CF, Madueno F, et al. 2006 How flower meristems are formed? Plant Mol. Biol. 60 855–870
Blazquez MA, Soowal LN, Lee I, et al. 1997 LEAFY expression and flower initiation in Arabidopsis. Development 124 3835–3844
Blixt S 1967 Linkage studies in Pisum VII. The manifestation of the genes cri and coch, and the double-recessive in Pisum. Agri Hort. Genet. 25 131–144
Blixt S 1972 Mutation genetics in Pisum. Agri Hort. Genet. 30 1–293
Bomblies K, Wang RL, Ambrose BA, et al. 2003 Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130 2385–2395
Bosch JA, Heo K, Sliwinski MK, et al. 2008 An exploration of LEAFY expression in independent evolutionary origins of rosette flowering in Brassicaceae. Am. J. Bot. 95 286–293
Bowman JL, Alvarez J, Weigel D, et al. 1993 Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119 721–743
Bradley D, Ratcliffe O, Vincent C, et al. 1997 Inflorescence commitment and architecture in Arabidopsis. Science 275 80–83
Calonje M, Sanchez R, Chen L, et al. 2008 EMBRYONIC FLOWER1 participates in polycomb group-mediated AG gene silencing in Arabidopsis. Plant Cell 20 277–291
Charlton WA 1991 Homoeosis and shoot construction in Azara microphylla Hook. (Flacourtiaceae). Acta Bot. Neerlandica 40 329–337
Cochran WG and Cox GM 1992 Experimental designs 2nd edition (John Wiley & Sons, Inc)
Condit R, Perez R and Daguerre N 2010 Trees of Panama and Costa Rica (New Jersey: Princeton University Press)
DeMason DA 2005 Extending Marx’s isogenic lines in search of Uni function. Pisum Genetics 37 10–14
DeMason DA and Chawla R 2004a Roles for auxin during morphogenesis of compound leaves of pea (Pisum sativum). Planta 218 435–448
DeMason DA and Chawla R 2004b Roles of auxin and Uni in leaf morphogenesis of afila genotype of pea (Pisum sativum). Int. J. Plant Sci. 165 707–722
DeMason DA and 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
DeMason DA and Villani PJ 2001 Genetic control of leaf development in pea (Pisum sativum). Int. J. Plant Sci. 162 493–511
de Vilmorin P and Bateson W 1911 A case of gametic coupling in Pisum. Proc. R. Soc. London Ser. B Biol. Sci. 84 9–11
Fawole I 2001 Genetic analysis of mutations at loci controlling leaf form in Cowpea (Vigna unguiculata [L] Walp.). J. Hered. 92 43–50
Ferrandiz C, Navarro C, Gomez MD, et al. 1999 Flower development in Pisum sativum: from the war of the whorls to the battle of common primordia. Dev. Genet. 25 280–290
Foucher F, Morin J, Courtiade J, et al. 2003 DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER 1/ CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15 2742–2754
Goldenberg JB 1965 Afila, a new mutant in pea (Pisum sativum L.). Boletin Genetico 1 27–31
Gourlay CW, Hofer JMI and Ellis THN 2000 Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, COCHLEATA, AFILA and TENDRIL-LESS. Plant Cell 12 1279–1294
Hanano S and Goto K 2011 Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcription repression. Plant Cell 23 3172–3184
Hempel FD, Weigel D, Mandel MA, et al. 1997 Floral determination and expression of floral regulatory genes in Arabidopsis. Development 124 3845–3853
Hepworth SR, Klenz JE and Haughn GW 2006 UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta 223 769–778
Hepworth SR, Zhang Y, McKim S, et al. 2005 BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. Development 17 1434–1448
Hirai M, Yamagishi M and Kanno A 2012 Reduced transcription of a LEAFY-like gene in Alstroemeria sp. cultivar Green Coral that cannot develop floral meristems. Plant Sci. 185–186 298–308
Hofer JMI, Gourlay CW and Ellis THN 2001 Genetic control of leaf morphology: a partial view. Ann. Bot. 88 1129–1139
Hofer J, Turner I, Hellens R, et al. 1997 UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7 581 587
Hofer J, Turner I, Moreau C, et al. 2009 Tendril-less regulates tendril formation in pea leaves. Plant Cell 21 420–428
Huala E and Sussex IM 1992 LEAFY interacts with floral homeotic genes to regulate Arabidopsis floral development. Plant Cell 4 901–913
Huijser P and Schmid M 2011 The control of developmental phase transitions in plants. Development 138 4117–4129
Irish VF 2010 The flowering of Arabidopsis flower development. Plant J. 61 1041–1028
Jack T. 2004 Molecular and genetic mechanisms of floral control. Plant Cell 16 S1–S17
Jinghua D, Fangdong L, Hongyan D, et al. 2012 Cloning and expression analysis of a LFY homologous gene in Chinese jujube (Ziziphus jujube Mill.). African J. Biotechnol. 11 581–589
Karim MR, Hirota A, Kwiatkowska D, et al. 2009 A role for Arabidopsis PUCH1 in floral meristem identity and bract suppression. Plant Cell 21 1360–1372
Kelly AJ, Bonnlander MB and Meeks-Wagner DR 1995 NFL, the tobacco homolog of FLORICAULA and LEAFY, is transcriptionally expressed in both vegetative and floral meristems. Plant Cell 7 225–234
Kobayashi Y and Weigel D 2007 Move on up, its time for change- Mobile signals controlling photoperiod-dependent flowering. Genes Dev. 21 2371–2384
Krizek BA and Fletcher JC 2005 Molecular mechanisms of flower development: An armchair guide. Nat, Rev, Genet. 6 688–698
Kumar A, Sharma V, Khan M, et al. 2012 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 DOI 10.1007/s00709-012-0397-3
Kumar S, Chaudhary S, Sharma V, et al. 2010 Genetic control of leaf-blade morphogenesis by the INSECATUS gene in Pisum sativum. J. Genet. 89 201–211
Kumar S, Mishra RK, Chaudhary S, et al. 2009a. Co-regulation of biomass partitioning by leafblade morphology genes AFILA, MULTIFOLIATE-PINNA, TENDRIL-LESS and UNIFOLIATA in grain pea Pisum sativum. Proc. Indian Nat. Sci. Acad. 75 15–25
Kumar S, Mishra RK, Kumar A, et al. 2009b. Regulation of stipule development by COCHLEATA and STIPULE-REDUCED genes in Pisum sativum. Planta 230 449–458
Kumar S, Rai SK, Pandey-Rai S, et al. 2004 Regulation of unipinnate character in the distal tendrilled domain of compound leafblade by the gene MULTIFOLIATE PINNA (MFP) in pea Pisum sativum. Plant Sci. 166 929–940
Kumar S and Sharma SB 1986 Mutations in three of the genes determining thiamine biosynthesis in Pisum sativum. Mol. General Genet. 204 473–476
Kumar S, Sharma V, Chaudhary S, et al. 2011 Interaction between COCHLEATA and UNIFOLIATA genes enables normal flower morphogenesis in the garden pea Pisum sativum. J. Genet. 90 309–314
Lamprecht H 1933 Ein unifoliata Typus von Pisum mit gleichzeitiger Pistilloidie. Hereditas 18 56–64
Lamprecht H 1959 Das Merkmal insecatus von Pisum und seine Vererbung sowie einige Koppelungsstudien. Agri Hort. Genet. 17 26–36
Lee I, Wolfe DS, Nilsson O, et al. 1997 A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr. Biol. 7 95–104
Lee JH, Lee JS and Ahn JH 2008 Ambient temperature signaling in plants: an emerging field in the regulation of flowering time. J. Plant Biol. 51 321–326
Levin JZ and Meyerowitz EM 1995 UFO: An Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7 529–548
Liljegren SJ, Gustafson-Brown C, Pinyopich A, et al. 1999 Interactions among APETALA1, LEAFY and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11 1007–1018
Liu C, Chen H, Ling Er H, et al. 2008 Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135 1481–1491
Liu T, Hu Y and Li X 2011 Characterization of a chestnut FLOURICAULA/LEAFY homologus gene. African J. Biotechnol. 10 3978–3985
Liu C, Xi W, Shen L, et al. 2009 Regulation of flower patterning by flowering time genes. Dev. Cell 16 711–722
Ma Y-P, Fang X-H, Chen F, et al. 2008 DFL a FLORICAULA/LEAFY homologue gene from Dendranthema lavandulifolium is expressed both in the vegetative and reproductive tissues. Plant Cell Rep. 27 647–654
Maizel A, Busch MA, Tanahashi T, et al. 2005 The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science 308 260–263
Mandel MA, Gustafson-Brown C, Savidge B, et al. 1992 Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360 273–277
Marx GA 1986 Tendrilled acacia (tac): an allele at the uni locus. Pisum Newslett. 18 49–52
Marx GA 1987 A suit of mutants that modify pattern formation in pea leaves. Plant Mol. Biol. Rep. 5 311–335
Michaels SD, Himelblau E, Kim SY, et al. 2005 Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 137 149–156
Mishra RK, Chaudhary S, Kumar A, et al. 2009 Effects of MULTIFOLIATE-PINNA, AFILA, TENDRIL-LESS and UNIFOLIATA genes on leafblade architecture in Pisum sativum. Planta 230 177–190
Molinero-Rosales N, Jamilena M, Zurita S, et al. 1999 FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J. 20 685–693
Monti LM, Devreux M. 1969 stamina pistilloida: a new mutation induced in pea. Theoretical and Applied Genetics 39 17–20
Moyroud E, Kusters E, Monniaux M, et al. 2010 LEAFY blossoms. Trend. Plant Sci. 15 346–352
Moyroud E, Minguet EG, Ott F, et al. 2011 Prediction of regulatory interactions from genome sequences using a biophysical model for the Arabidopsis LEAFY transcription factor. Plant Cell 23 1293–1306
Moyroud E, Tichtinsky G and Parcy F 2009 The LEAFY floral regulators in Angiosperms: conserved proteins with diverse roles. J. Plant Biol. 52 177–185
Myers JR and Bassett MJ 1993 Inheritance, allellsm, and morphological characterization of unlfoliate mutations in common bean. J. Hered. 84 17–20
Ng M and Yanofsky MF 2001 Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13 739–753
Nougarede A and Rondet P 1973 Les, stipules du Pisum sativum L var. nain hatif d Annonay et leurs relations avec la feuille a l’etat jeune. Compte Rendu de l’ Academie des Sciences de Paris, serie D. 277 393–396
Parcy F 2005 Flowering: A time for integration. Int. J. Dev. Biol. 49 585–593
Parcy F, Bomblies K and Weigel D 2002 Interaction of LEAFY, AGAMOUS and TERMINAL FLOWER1 in maintaining floral meristem identity in Arabidopsis. Development 129 2519–2527
Parcy F, Nilsson O, Busch MA, et al. 1998 A genetic framework for floral patterning. Nature 395 561–566
Pastore JJ, Limpuangthip A, Yamaguchi N, et al. 2011 LATE MERISTEM IDENTITY2 acts together with LEAFY to activate APETALA1. Development 138 3189–3198
Pellew C and Sverdrup A 1923 New observations on the genetics of peas (Pisum sativum). J. Genet. 13 125–131
Poethig RS 2003 Phase change and the regulation of developmental timing in plants. Science 301 334–336
Prajapati S and 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
Prenner G, Cacho NI, Baum D, et al. 2010 Is LEAFY a useful marker gene for the flower- inflorescence boundary in the Euphorbia cyathium? J. Exp. Bot. 62 345–350
Rao NN, Prasad K, Kumar PR, et al. 2008 Distinct regulatory role for RFL, the rice LFY homolog, in determining flowering time and plant architecture. Proc. Nat. Acad. Sci. USA 105 3646–3651
Rutishauser R 1999 Polymerous leaf whorls in vascular plants: developmental morphology and fuzziness of organ identity. Int. J. Plant Sci. 160 S81–S103
Rutishauser R, Grob V and Pfeifer E 2008 Plants are used to having identity crises; in Key themes in evolutionary developmental biology (eds) A Minelli and G Fusco (Cambridge: Cambridge University Press) pp 194–213
Sattler R and Rutishauser R 1997 The fundamental relevance of morphology and morphogenesis to plant research. Ann. Bot. 80 571–582
Schultz EA and Haughn GW 1991 LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3 771–781
Schmittgen TD and Livak KJ 2008 Analyzing real-time PCR data by the comparative C T method. Nat. Protocol. 3 1101–1108
Shannon S and Meeks-Wagner DR 1991 A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3 877–892
Sharma B 1981 Genetic pathway of foliage development in Pisum sativum. Pulse Crops Newslett. 1 26–32
Sharma B and Kumar S 1981 Discovery of one more allele of the tac-locus of Pisum sativum. Pulse Crops Newslett. 4 50
Sharma V, Tripathi BN and Kumar S 2012 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 System. Evol. 298 1167–1175
Shistukawa N, Takagishi A, Ikari C, et al. 2006 A wheat FLORICAULA/LEAFY ortholg, is associated with spikelet formation as lateral branch of the inflorescence meristem. Genes Genet. Syst. 81 13–20
Singer S, Sollinger J, Maki S, et al. 1999 Inflorescence architecture: A developmental genetics approach. Bot. Rev. 65 385–410
Smirnova OG 2002 Characteristics and inheritance of the leaf mutation ins. Pisum Genet. 34 34–35
Sooda A, Song J, Jameson PE, et al. 2011 Phase change and flowering in Pachycladon exile and isolation of LEAFY and TERMINAL FLOWER 1 homologus. New Zeal. J. Bot. 49 281–293
Souer E, Rebocho AB, Bliek M, et al. 2008 Patterning of inflorescences and flowers by the F-box protein DOUBLE TOP and the LEAFY homolog ABERRANT LEAF AND FLOWER of Petunia. Plant Cell 20 2033–2048
Steeves TA and Sussex I 1989 Pattern in plant development (Cambridge: Cambridge University Press)
Swiecicki WK 1987 determinate growth (det) in Pisum: A new mutant gene on chromosome 7. Pisum Newslett. 19 72–73
Taylor S, Hofer J and 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
Tyler AA 1897 The nature and origin of stipules. Ann. NY Acad. Sci. 10 1–49
Wagner D, Sablowski RW and Meyerowitz EM 1999 Transcriptional activation of APETALA1 by LEAFY. Science 285 582–584
Wang H, Chen J, Wen J, et al. 2008 Control of compound leaf development by FLOURICAULA/LEAFY ortholog SINGLE LEAFLET 1 in Medicago truncatula. Plant Physiol. 146 1759–1779
Weigel D, Alvarez J, Smyth DR, et al. 1992 LEAFY controls floral meristem identity in Arabidopsis. Cell 67 843–859
Weigel D and Nilsson O 1995 A developmental switch sufficient for flower initiation in diverse plants. Nature 377 495–500
Wilkinson MD and Haughn GW 1995 UNUSUAL FLORAL ORGANS controls meristem identity and organ primordial fate in Arabidopsis. Plant Cell 7 1485–1499
William DA, Su Y, Smith ML, et al. 2004 Genomic identification of direct target genes of LEAFY. Proc. Nat. Acad. Sci. USA 101 1775–1780
Winter CM, Austin RS, Blavillain-Baufume S, et al. 2011 LEAFY target genes reveal floral regulatory logic, cis motifs and a link to biotic stimulus response. Cell 20 430–433.
Yamaguchi A, Wu MF, Yang L, et al. 2009 The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev. Cell 17 268–278
Yamaguchi N, Yamaguchi A, Abe M, et al. 2012 LEAFY controls Arabidopsis pedicel length and orientation by affecting adaxial-abaxial cell fate. Plant J. 69 844–856
Yaxley JL, Jablonski W and Reid JB 2001 Leaf and flower development in pea (Pisum sativum L.): mutants cochleata and unifoliata. Ann. of Bot. 88 225–234
Acknowledgements
We wish to acknowledge support of the Director, NIPGR, in terms of provision of research facilities and help provided by Vinod Kumar in field crop management. The research was funded by Indian National Science Academy and Council of Scientific and Industrial Research (CSIR, India) grants to SK and postgraduate fellowship grants from CSIR to SC and SK and from SKA Institution for Research, Education and Development to VS. We also wish to thank Susan Singer for the highly useful discussion via email and Anand Sarkar and Bithika Sharma for reading the manuscript.
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[Sharma V, Chaudhary S, Kumar A and Kumar S 2012 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
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Sharma, V., Chaudhary, S., Kumar, A. et al. COCHLEATA controls leaf size and secondary inflorescence architecture via negative regulation of UNIFOLIATA (LEAFY ortholog) gene in garden pea Pisum sativum . J Biosci 37 (Suppl 1), 1041–1059 (2012). https://doi.org/10.1007/s12038-012-9263-x
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DOI: https://doi.org/10.1007/s12038-012-9263-x