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Molecular cloning, phylogenetic analysis, and expression patterns of LATERAL SUPPRESSOR-LIKE and REGULATOR OF AXILLARY MERISTEM FORMATION-LIKE genes in sunflower (Helianthus annuus L.)

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Abstract

The wild sunflower (Helianthus annuus) plants develop a highly branched form with numerous small flowering heads. The origin of a no branched sunflower, producing a single large head, has been a key event in the domestication process of this species. The interaction between hormonal factors and several genes organizes the initiation and outgrowth of axillary meristems (AMs). From sunflower, we have isolated two genes putatively involved in this process, LATERAL SUPPRESSOR (LS)-LIKE (Ha-LSL) and REGULATOR OF AXILLARY MERISTEM FORMATION (ROX)-LIKE (Ha-ROXL), encoding for a GRAS and a bHLH transcription factor (TF), respectively. Typical amino acid residues and phylogenetic analyses suggest that Ha-LSL and Ha-ROXL are the orthologs of the branching regulator LS and ROX/LAX1, involved in the growth habit of both dicot and monocot species. qRT-PCR analyses revealed a high accumulation of Ha-LSL transcripts in roots, vegetative shoots, and inflorescence shoots. By contrast, in internodal stems and young leaves, a lower amount of Ha-LSL transcripts was observed. A comparison of transcription patterns between Ha-LSL and Ha-ROXL revealed some analogies but also remarkable differences; in fact, the gene Ha-ROXL displayed a low expression level in all organs analyzed. In situ hybridization (ISH) analysis showed that Ha-ROXL transcription was strongly restricted to a small domain within the boundary zone separating the shoot apical meristem (SAM) and the leaf primordia and in restricted regions of the inflorescence meristem, beforehand the separation of floral bracts from disc flower primordia. These results suggested that Ha-ROXL may be involved to establish a cell niche for the initiation of AMs as well as flower primordia. The accumulation of Ha-LSL transcripts was not restricted to the boundary zones in vegetative and inflorescence shoots, but the mRNA activity was expanded in other cellular domains of primary shoot apical meristem as well as AMs. In addition, Ha-LSL transcript accumulation was also detected in leaves and floral primordia at early stages of development. These results were corroborated by qRT-PCR analyses that evidenced high levels of Ha-LSL transcripts in very young leaves and disc flowers, suggesting a role of Ha-LSL for the early outgrowth of lateral primordia.

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References

  • Agusti J, Greb T (2013) Going with the wind—adaptive dynamics of plant secondary meristems. Mech Dev 130:34–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barthélémy D, Caraglio Y (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann Bot 99:375–407

    Article  PubMed  PubMed Central  Google Scholar 

  • Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341:95–113

    Article  CAS  PubMed  Google Scholar 

  • Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL (2002) The pfam protein families database. Nucleic Acids Res 30:276–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baute GJ, Kane NC, Grassa CJ, Lai Z, Rieseberg LH (2015) Genome scans reveal candidate domestication and improvement genes in cultivated sunflower, as well as post-domestication introgression with wild relatives. New Phytol 206:830–838

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bennett T, Leyser O (2006) Something on the side: axillary meristems and plant development. Plant Mol Biol 60:843–854

    Article  CAS  PubMed  Google Scholar 

  • Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16:553–563

    Article  CAS  PubMed  Google Scholar 

  • Beveridge CA, Kyozuka J (2010) New genes in the strigolactone-related shoot branching pathway. Curr Opin Plant Biol 13:34–39

    Article  CAS  PubMed  Google Scholar 

  • Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692

    Article  CAS  PubMed  Google Scholar 

  • Burian A, de Reuille PB, Kuhlemeier C (2016) Patterns of stem cell divisions contribute to plant longevity. Curr Biol 26:1385–1394

    Article  CAS  PubMed  Google Scholar 

  • Burke JM, Knapp SJ, Rieseberg LH (2005) Genetic consequences of selection during the evolution of cultivated sunflower. Genetics 171:1933–1940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng X, Ruyter-Spira C, Bouwmeester H (2013) The interaction between strigolactones and other hormones in the regulation of plant development. Front Plant Sci 4:199

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Zhao Y (2007) A role for auxin in flower development. J Integ Plant Biol 49:99–104

    Article  CAS  Google Scholar 

  • Cline MG (1991) Apical dominance. Bot Rev 57:318–358

    Article  Google Scholar 

  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488

    Article  CAS  PubMed  Google Scholar 

  • Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321

    Article  CAS  PubMed  Google Scholar 

  • Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nature Rev Mol Cell Biol 12:211–221

    Article  CAS  Google Scholar 

  • Drummond RS, Janssen BJ, Luo Z, Oplaat C, Ledger SE, Wohlers MW, Snowden KC (2015) Environmental control of branching in petunia. Plant Physiol 168:735–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96

    Article  CAS  PubMed  Google Scholar 

  • Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJ, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30:235–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fambrini M, Cionini G, Bertini D, Michelotti V, Conti A, Pugliesi C (2003) MISSING FLOWERS gene controls axillary meristems initiation in sunflower. Genesis 36:25–33

    Article  CAS  PubMed  Google Scholar 

  • Fambrini M, Durante C, Cionini G, Geri C, Giorgetti L, Michelotti V, Salvini M, Pugliesi C (2006) Characterization of LEAFY COTYLEDON1-LIKE gene in Helianthus annuus and its relationship with zygotic and somatic embryogenesis. Dev Genes Evol 216:253–264

    Article  CAS  PubMed  Google Scholar 

  • Fambrini M, Mariotti L, Parlanti S, Salvini M, Pugliesi C (2015) A GRAS-like gene of sunflower (Helianthus annuus L.) alters the gibberellin content and axillary meristem outgrowth in transgenic Arabidopsis plants. Plant Biol 17:1123–1134

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gallavotti A, Zhao Q, Kyozuka J, Meeley RB, Ritter MK, Doubley JF, Pè MP, Schmidt RJ (2004) The role of barren stalk1 in the architecture of maize. Nature 432:630–635

    Article  CAS  PubMed  Google Scholar 

  • Grbic V (2005) Comparative analysis of axillary and floral meristem development. Can J Bot 83:343–349

    Article  Google Scholar 

  • Greb T, Clarenz O, Schäfer E, Muller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes & Dev 17:1175–1187

    Article  CAS  Google Scholar 

  • Heery DM, Kalkhoven E, Hoare S, Parker MG (1997) A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733–736

    Article  CAS  PubMed  Google Scholar 

  • Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20:735–747

    Article  CAS  PubMed  Google Scholar 

  • Heiser CB (1976) The sunflower. University of Oklahoma Press, Norman, OK

    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  CAS  PubMed  Google Scholar 

  • Hirano K, Asano K, Tsuji H, Kawamura M, Mori H, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2010) Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. Plant Cell 22:2680–2696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hockett EA, Knowles PF (1970) Inheritance of branching in sunflowers, Helianthus annuus L. Crop Sci 10:432–436

    Article  Google Scholar 

  • IBPGR (1985) Descriptors for cultivated and wild sunflower. AGPG, /85/54, ROME

  • Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellins signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson D (1991) In situ hybridisation in plants. In: Bowles DJ, Gurr GJ, McPherson M (eds) Molecular plant pathology: a practical approach. Oxford University Press, Oxford, pp 163–174

    Google Scholar 

  • Janssen BJ, Drummond RSM, Snowden KC (2014) Regulation of axillary shoot development. Curr Opin Plant Biol 17:28–35

    Article  PubMed  Google Scholar 

  • Keller T, Abbott J, Moritz T, Doerner P (2006) Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development. Plant Cell 18:598–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I, Okamoto H, Shimamoto K, Kyozuka J (2003) LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci U S A 100:11765–11770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee MH, Kim B, Song SK, Heo JO, Yu NI, Lee SA, Kim M, Kim DG, Sohn SO, Lim CE, Chang KS, Lee MM, Lim J (2008) Large-scale analysis of the GRAS gene family in Arabidopsis thaliana. Plant Mol Biol 67:659–670

    Article  CAS  PubMed  Google Scholar 

  • Leyser O (2009) The control of shoot branching: an example of plant information processing. Plant Cell & Env 32:694–703

    Article  CAS  Google Scholar 

  • Li X, Qian Q, Fu Z, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Widmer A (2014) Genome-wide comparative analysis of the GRAS gene family in Populus, Arabidopsis and rice. Plant Mol Biol Rep 32:1129–1145

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Wang T, Xu Z, Sun L, Zhang Q (2014) Genome-wide analysis of the GRAS gene family in Prunus mume. Mol Gen Genomics 290:303–317

    Article  Google Scholar 

  • Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39

    Article  PubMed  Google Scholar 

  • Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci U S A 111:6092–6097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller J, Fick G (1997) The genetics of sunflower. In: Schneiter AA (ed) Sunflower technology and production, agronomy monography no 35. CSSA, Madison, WI, pp 441–495

    Google Scholar 

  • Müller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18:586–597

    Article  PubMed  PubMed Central  Google Scholar 

  • Oikawa T, Kyozuka J (2009) Two-step regulation of LAX PANICLE1 protein accumulation in axillary meristem formation in rice. Plant Cell 21:1095–1108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Przemeck GKH, Mattsson J, Hardtke CS, Sung ZR, Berleth T (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200:229–237

    Article  CAS  PubMed  Google Scholar 

  • Pugliesi C, Salvini M, Fambrini M (2013) Isolation and molecular analysis of two R2R3-MYB genes from the sunflower (Helianthus annuus). Botany 91:731–738

    Article  CAS  Google Scholar 

  • Putt ED (1964) Recessive branching in sunflowers. Crop Sci 4:444–445

    Article  Google Scholar 

  • Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119

    Article  CAS  PubMed  Google Scholar 

  • Rameau C, Bertheloot J, Leduc N, Andrieu B, Foucher F, Sakr S (2015) Multiple pathways regulate shoot branching. Front Plant Sci 5:741

    Article  PubMed  PubMed Central  Google Scholar 

  • Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhardt D, Kuhlemeier C (2002) Plant architecture. EMBO Rep 3:846–851

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Rossmann S, Kohlen W, Hasson A, Theres K (2015) Lateral suppressor and goblet act in hierarchical order to regulate ectopic meristem formation at the base of tomato leaflets. Plant J 81:837–848

    Article  CAS  PubMed  Google Scholar 

  • Sandu I, Vrânceanu AV, Pãcureanu-Joiþa M (1999) Analysis of the genetic control of branching types in sunflower (Helianthus annuus L.). Romanian Agric Res 11-12:17–19

    Google Scholar 

  • Sassi M, Vernoux T (2013) Auxin and self-organization at the shoot apical meristem. J Exp Bot 64:2579–2592

    Article  CAS  PubMed  Google Scholar 

  • Schmitz G, Tillmann E, Carriero F, Fiore C, Cellini F, Theres K (2002) The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc Natl Acad Sci U S A 99:1064–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci U S A 96:290–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu-Sato S, Mori H (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol 127:1405–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverstone AL, Ciampaglio CN, Sun TP (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. Freeman, San Francisco, CA

    Google Scholar 

  • Snow R (1929) The young leaf as the inhibiting organ. New Phytol 28:345–358

    Article  Google Scholar 

  • Song XM, Liu TK, Duan WK, Ma QH, Ren J, Wang Z, Li Y, Hou XL (2014) Genome-wide analysis of the GRAS gene family in Chinese cabbage (Brassica rapa ssp. pekinensis). Genomics 103:135–146

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Xue B, Jones WT, Rikkerink E, Dunker AK, Uversky VN (2011) A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development. Plant Mol Biol 77:205–223

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Jones TW, Rikkerink EHA (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signaling. Biochem J 442:1–12

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Rikkerink EHA, Jones WT, Uversky VN (2013) Multifarious roles of intrinsic disorder in protein illustrate its broad impact on plant biology. Plant Cell 25:38–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sussex IM, Kerk NM (2001) The evolution of plant architecture. Curr Opin Plant Biol 4:33–37

    Article  CAS  PubMed  Google Scholar 

  • Szymkowiak EJ, Sussex IM (1993) Effect of lateral suppressor on petal initiation in tomato. Plant J 4:1–7

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Taylor-Teeples M, Lanctot A, Nemhauser JL (2016) As above, so below: auxin’s role in lateral organ development. Dev Biol 419:156–164

    Article  CAS  PubMed  Google Scholar 

  • Thimann KV, Skoog F (1933) Studies on the growth hormone of plants: III. The inhibiting action of the growth substance on bud development. Proc Natl Acad Sci U S A 19:714–716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian C, Jiao Y (2015) A systems approach to understand shoot branching. Curr Plant Biol 3-4:13–19

    Article  Google Scholar 

  • Uberti Monassero NG, Viola IL, Welchen E, Gonzalez DH (2013) TCP transcription factors: architectures of plant form. Biomol Concepts 4:11–127

    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

    CAS  PubMed  Google Scholar 

  • Wang Q, Kohlen W, Rossmann S, Vernoux T, Theres K (2014a) Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato. Plant Cell 26:2068–2079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Hasson A, Rossmann S, Theres K (2016) Divide et impera: boundaries shape the plant body and initiate new meristems. New Phytol 209:485–498

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59:253–279

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wang J, Shi B, Yu T, Qi J, Meyerowitz EM, Jiao Y (2014b) The stem cell niche in leaf axils is established by auxin and cytokinin in Arabidopsis. Plant Cell 26:2055–2067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woods DP, Hope CL, Malcomber ST (2011) Phylogenomic analyses of the BARREN STALK1/LAX PANICLE1 (BA1/LAX1) genes and evidence for their roles during axillary meristem development. Mol Biol Evol 28:2147–2159

    Article  CAS  PubMed  Google Scholar 

  • Wu N, Zhu Y, Song W, Li Y, Yan Y, Hu Y (2014) Unusual tandem expansion and positive selection in subgroups of the plant GRAS transcription factor superfamily. BMC Plant Biol 14:373

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu X, McSteen P (2007) The role of auxin transport during inflorescence development in maize, Zea mays (Poaceae). Am J Bot 11:1745–1755

    Article  Google Scholar 

  • Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN (2010) PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochim Biophys Acta 1804:996–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang F, Wang Q, Schmitz G, Müller D, Theres K (2012) The bHLH protein ROX acts in concert with RAX1 and LAS to modulate axillary meristem formation in Arabidopsis. Plant J 71:61–70

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Jiao Y (2016) Regulation of axillary meristem initiation by transcription factors and plant hormones. Front Plant Sci 7:183

    PubMed  PubMed Central  Google Scholar 

  • Yuan L-H, Pan J-S, Wang G, Zhu J, Zhang W-W, Li Z, He H-L (2010) The Cucumber Lateral Suppressor gene (CLS) is functionally associated with axillary meristem initiation. Plant Mol Biol Rep 28:421–429

    Article  CAS  Google Scholar 

  • Žádníková P, Simon R (2014) How boundaries control plant development. Curr Opin Plant Biol 17:116–125

    Article  PubMed  Google Scholar 

  • Zhang B, Liu X, Xu W, Chang J, Li A, Mao X, Zhang X, Jing R (2015) Novel function of a putative MOC1 ortholog associate with spikelet number per spike in common wheat. Sci Rep 5:12211

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Iyer LM, Aravind L (2012) Bacterial GRAS domain proteins throw new light on gibberellic acid response mechanisms. Bioinformatics 28:2407–2411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving Genes and Proteins. Academic Press, New York, NY, pp 97–166

    Chapter  Google Scholar 

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  1. Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy

    Marco Fambrini, Mariangela Salvini & Claudio Pugliesi

  2. Scuola Normale Superiore, Piazza dei Cavalieri 7, 56126, Pisa, Italy

    Mariangela Salvini

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  1. Marco Fambrini
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  2. Mariangela Salvini
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Fambrini, M., Salvini, M. & Pugliesi, C. Molecular cloning, phylogenetic analysis, and expression patterns of LATERAL SUPPRESSOR-LIKE and REGULATOR OF AXILLARY MERISTEM FORMATION-LIKE genes in sunflower (Helianthus annuus L.). Dev Genes Evol 227, 159–170 (2017). https://doi.org/10.1007/s00427-016-0571-2

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