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CaBLIND regulates axillary meristem initiation and transition to flowering in pepper

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Abstract

Plant architecture is a major motif in plant diversity. The shape of the plant is regulated by genes that have been found to have similar or related functions in different species. However, changes in gene regulation or their recruitment to additional developmental pathways contribute to the wide range of plant patterns. Our aim was to unravel the genetic mechanisms governing the unique architecture of pepper (Capsicum annuum) and to determine whether these genetic factors have conserved functions in other plant species. We describe the pepper CaBLIND (CaBL) gene that is orthologous to the tomato (Solanum lycopersicum) BLIND (BL) and to the Arabidopsis thaliana REGULATOR OF AXILLARY MERISTEMS (RAX). We identified two allelic Cabl mutants that show dramatic reduction in axillary meristem initiation. In addition, Cabl exhibits late flowering and ectopic vegetative growth during the reproductive phase. Double-mutant and expression analyses suggest that CaBL functions independently of FASCICULATE, the pepper ortholog of SELF PRUNING in regulating sympodial growth, but is epistatic to FASCICULATE in controlling axillary meristem formation. Furthermore, CaBL operates independently of CaREVOLUTA and CaLATERAL SUPPRESSOR in regulating axillary branching. Our results provide evidence of CaBL’s conserved function with BL and RAX genes in regulating axillary meristem initiation early in development. In addition, similar to BL but opposite to RAX, CaBL acts to promote the transition from vegetative to reproductive phase. However, in contrast to BL and RAX, CaBL is co-opted to play a role in suppressing vegetative growth during the reproductive phase in pepper.

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Abbreviations

AM:

Axillary meristems

BL:

BLIND

CaBL:

Capsicum annuum BLIND

EMS:

Ethyl methanesulfonate

FA:

FASCICULATE

GA:

Gibberellic acid

LS:

Lateral suppressor

RAX:

REGULATOR OF AXILLARY MERISTEMS

REV:

REVOLUTA

SAM:

Shoot apical meristem

SEM:

Scanning electron microscope

SP:

SELF PRUNING

TFL1:

TERMINAL FLOWER1

References

  • Ben Chaim A, Paran I, Grube RC, Jahn M, van Wijk R, Peleman J (2001) QTL mapping of fruit-related traits in pepper (Capsicum annuum). Theor Appl Genet 102:1016–1028

    Article  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 

  • David-Schwartz R, Sinha N (2007) Evolution and development in plants: bridging the gap. Int J Plant Sci 168:49–59

    Article  CAS  Google Scholar 

  • Elitzur T, Nahum H, Borovsky Y, Pekker I, Eshed Y, Paran I (2009) Co-ordinated regulation of flowering time, plant architecture and growth by FASCICULATE: the pepper orthologue of SELF PRUNING. J Exp Bot 60:869–880

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Greb T, Clarenz O, Schafer 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  PubMed  CAS  Google Scholar 

  • Hirsch S, Oldroyd GED (2009) GRAS-domain transcription factors that regulate plant development. Plant Signal Behav 4:698–700

    Article  PubMed  CAS  Google Scholar 

  • Johansen DA (1940) Plant microtechniques. McGraw-Hill Book, New York

    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  PubMed  CAS  Google Scholar 

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  PubMed  CAS  Google Scholar 

  • Lee MM, Schiefelbein J (2001) Developmentally distinct MYB genes encode functionally equivalent proteins in Arabidopsis. Development 128:1539–1546

    PubMed  CAS  Google Scholar 

  • Li X, Qian Q, Fu Z, Wang Y, 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  PubMed  CAS  Google Scholar 

  • Mapelli S, Kinet J-M (1992) Plant growth regulator and graft control of axillary bud formation and development in the TO-2 mutant tomato. Plant Growth Regul 11:385–390

    Article  CAS  Google Scholar 

  • Michael MN, Joseph DN, Joanne C, Alan EP (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25:223–236

    Article  PubMed  CAS  Google Scholar 

  • Paran I, Borovsky Y, Nahon S, Cohen O (2007) The use of induced mutations to study shoot architecture in Capsicum. Israel J Plant Sci 55:125–131

    Article  Google Scholar 

  • Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989

    PubMed  CAS  Google Scholar 

  • Pnueli L, Gutfinger T, Hareven D, Ben-Naim O, Ron N, Adir N, Lifschitz E (2001) Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell 13:2687–2702

    Article  PubMed  CAS  Google Scholar 

  • Quinet M, Dielen V, Batoko H, Boutry M, Havelange A, Kinet J-M (2006) Genetic interactions in the control of flowering time and reproductive structure development in tomato (Solanum lycopersicum). New Phytol 170:701–710

    Article  PubMed  CAS  Google Scholar 

  • Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55:65–76

    Article  PubMed  CAS  Google Scholar 

  • Schmitz G, Theres K (1999) Genetic control of branching in Arabidopsis and tomato. Curr Opin Plant Biol 2:51–55

    Article  PubMed  CAS  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 Nat Acad Sci USA 99:1064–1069

    Article  PubMed  CAS  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 Nat Acad Sci USA 96:290–295

    Article  PubMed  CAS  Google Scholar 

  • Snow M, Snow R (1942) The determination of axillary buds. New Phytol 41:13–22

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Szymkowiak EJ, Irish EE (1999) Interactions between jointless and wild-type tomato tissues during development of the pedicel abscission zone and the inflorescence meristem. Plant Cell 11:159–176

    Article  PubMed  CAS  Google Scholar 

  • Talbert PB, Adler HT, Parks DW, Comai L (1995) The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121:2723–2735

    PubMed  CAS  Google Scholar 

  • Tucker DJ (1976) Endogenous growth regulators in relation to side shoot development in the tomato. New Phytol 77:561–568

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Saadia Nahon for his technical support, Oded Cohen for FA expression analysis and useful discussions throughout the work, Arnon Brand for graphic design in Fig. 1, and also Hanita Zemach for assistance with microscopic analyses. We thank Doil Choi for sharing pepper sequence data with us. This research was supported by The Israel Science Foundation (Grant No. 1349/10).

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Authors and Affiliations

  1. Institute of Plant Science, The Volcani Center, Agricultural Research Organization, P.O. Box 6, 50250, Bet Dagan, Israel

    Dar Jeifetz, Rakefet David-Schwartz, Yelena Borovsky & Ilan Paran

  2. The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel

    Rakefet David-Schwartz

Authors
  1. Dar Jeifetz
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  2. Rakefet David-Schwartz
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  3. Yelena Borovsky
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  4. Ilan Paran
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Correspondence to Ilan Paran.

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D. Jeifetz and R. David-Schwartz contributed equally to this manuscript.

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Supplemental Fig. 1S

Expression analysis of CaREV and CaLS in wild type and Cabl. a, b Real-time RT-PCR analysis of CaREV (a) and CaLS (b) expression in wild-type (WT) and Cabl pepper plants in two-leaf (vegetative meristem) and six-leaf (transition to flowering) growth phases. UBIQUITN expression values were used to normalize the expression level of CaREV. Error bars denote standard error over three biological replicates. (31 kb)

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Jeifetz, D., David-Schwartz, R., Borovsky, Y. et al. CaBLIND regulates axillary meristem initiation and transition to flowering in pepper. Planta 234, 1227–1236 (2011). https://doi.org/10.1007/s00425-011-1479-8

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  • DOI: https://doi.org/10.1007/s00425-011-1479-8

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