Abstract
Knotted-like homeobox (KNOX) genes encode important regulators of shoot development in flowering plants. In Arabidopsis, class I KNOX genes are part of a regulatory system that contributes to indeterminacy of shoot development, delimitation of leaf primordia and internode development. In other species, class I KNOX genes have also been recruited in the control of marginal blastozone fractionation during dissected leaf development. Here we report the isolation of class I KNOX genes from two species of the basal eudicot family Papaveraceae, Chelidonium majus and Eschscholzia californica. Sequence comparisons and expression patterns indicate that these genes are orthologs of SHOOTMERISTEMLESS (STM), a class I KNOX gene from Arabidopsis. Both genes are expressed in the center of vegetative and floral shoot apical meristems (SAM), but downregulated at leaf or floral organ initiating sites. While Eschscholzia californica STM (EcSTM) is again upregulated during acropetal pinna formation, in situ hybridization could not detect Chelidonium majus STM (CmSTM) transcripts at any stage of basipetal leaf development, indicating divergent evolution of STM gene function in leaves within Papaveraceae. Immunolocalization of KNOX proteins indicate that other gene family members may control leaf dissection in both species. The contrasting direction of pinna initiation in the two species was also investigated using Histone H4 expression. Leaves at early stages of development did not reveal notable differences in cell division activity of the elongating leaf axis, suggesting that differential meristematic growth may not play a role in determining the observed dissection patterns.
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Abbreviations
- KNOX :
-
Knotted-like homeobox
- STM :
-
Shootmeristemless
- CmSTM :
-
Chelidonium majus STM
- EcSTM :
-
Eschscholzia californica STM
- FLO/LFY :
-
Floricaula/Leafy
- SAM:
-
shoot apical meristem
- KNAT :
-
KNOTTED-like from Arabidopsis thaliana
- Bp :
-
brevipedicellus
- LP:
-
leaf primordium
- RT-PCR:
-
Reverse transcription polymerase chain reaction
- RACE:
-
Rapid amplification of cDNA ends
- PsKn1 :
-
Pisum sativum knotted1
- LeT6 :
-
Lycopersicon esculentum T6
- TKn1 :
-
Tomato Knotted1
- PP:
-
pinna primordium
References
G. Bharathan B. Janssen E.A. Kellogg N. Sinha (1999) ArticleTitlePhylogenetic relationships and evolution of the KNOTTED class of plant homeodomain proteins Mol. Biol. Evol. 16 553–563
G. Bharathan T. Goliber C. Moore S. Kessler T. Pham N. Sinha (2002) ArticleTitleHomologies in leaf form inferred from KNOX1 gene expression during development Science 296 1858–1860
M.A. Blázquez L.N. Soowal I. Lee D. Weigel (1997) ArticleTitleLEAFY expression and flower initiation in Arabidopsis Development 124 3835–3844
J. Brandstädter C. Rossbach K. Theres (1994) ArticleTitleThe pattern of Histone H4 expression in the tomato shoot apex changes during development Planta 192 69–74
A. Busch S. Gleissberg (2003) ArticleTitleEcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex Planta 217 841–848
M.J. Carmona P. Cubas J.M. Martinez-Zapater (2002) ArticleTitleVFL, the grapevine FLORICAULA/LEAFY ortholog, is expressed in meristematic regions independently of their fate Plant Physiol. 130 68–77
C.E.M. Champagne N.W. Ashton (2001) ArticleTitleAncestry of KNOX genes revealed by bryophyte (Physcomitrella patens) homologs New Phytol. 150 23–36
J.J. Chen B.J. Janssen A. Williams N. Sinha (1997) ArticleTitleA gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution Plant Cell 9 1289–1304
H.T. Cho D.J. Cosgrove (2000) ArticleTitleAltered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 97 9783–9788
G. Chuck C. Lincoln S. Hake (1996) ArticleTitleKNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis Plant Cell 8 1277–1289
A.D. Deshpande W. Ramakrishna G.P. Mulay V.S. Gupta P.K. Ranjekar (1999) ArticleTitlePhylogenetic classification and molecular evolution of knotted1 homeobox genes Theor. Appl. Gen. 99 203–209
S.J. Douglas G. Chuck R.E. Dengler L. Pelecanda C.D. Riggs (2002) ArticleTitleKNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis Plant Cell 14 547–588
J.L. Gallois C. Woodward G.V. Reddy R. Sablowski (2002) ArticleTitleCombined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis Development 129 3207–3217
S. Gleissberg (1998) ArticleTitleComparative analysis of leaf shape development in Papaveraceae–Chelidonioideae Flora 193 387–409
S. Gleissberg (2004) ArticleTitleComparative analysis of leaf shape development in Eschscholzia californica and other Papaveraceae–Eschscholzioideae Am. J. Bot. 91 306–312
S. Gleissberg J.W. Kadereit (1999) ArticleTitleEvolution of leaf morphogenesis: Evidence from developmental and phylogenetic data in Papaveraceae Intl. J. Plant Sci. 160 787–794
W. Hagemann S. Gleissberg (1996) ArticleTitleOrganogenetic capacity of leaves: the significance of marginal blastozones in angiosperms Plant Syst. Evol. 199 121–152
J. Hofer L. Turner R. Hellens M. Ambrose P. Matthews A. Michael N. Ellis (1997) ArticleTitleUNIFOLIATA regulates leaf and flower morphogenesis in pea Curr. Biol. 7 581–587
J. Hofer C. Gourlay A. Michael T.H.N. Ellis (2001) ArticleTitleExpression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia Plant Mol. Biol. 45 387–398
B.J. Janssen A. Williams J.J. Chen J. Mathern S. Hake N. Sinha (1998a) ArticleTitleIsolation and characterization of two knotted-like homeobox genes from tomato Plant Mol. Biol. 36 417–425
B.J. Janssen L. Lund N. Sinha (1998b) ArticleTitleOverexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf Plant Physiol. 117 771–786
P. Kenrick P.R. Crane (1997) The Origin and Early Diversification of Land Plants Smithsonian Institution Press Washington
R. Kerstetter E. Vollbrecht B. Lowe B. Veit J. Yamaguchi S. Hake (1994) ArticleTitleSequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes Plant Cell 6 1877–1887
M. Kim T. Pham A. Hamidi S. McCormick R.K. Kuzoff N. Sinha (2003) ArticleTitleReduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves Development 130 4405–4415
H. Koltai D.M. Bird (2000) ArticleTitleEpistatic repression of PHANTASTICA and class 1 KNOTTED genes is uncoupled in tomato Plant J. 22 455–459
C. Lincoln J. Long J. Yamaguchi S. Hake (1994) ArticleTitleA knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants Plant Cell 6 1859–1876
J.A. Long E.I. Moan J.I. Medford M.K. Barton (1996) ArticleTitleA member of the KNOTTED class of homeodomain proteins encoded by the SHOOTMERISTEMLESS gene of Arabidopsis Nature 379 66–69
J. Long M.K. Barton (2000) ArticleTitleInitiation of axillary and floral meristems in Arabidopsis Dev. Biol. 218 341–353
W.P. Maddison D.R. Maddison (2000) MacClade version 4: Analysis of Phylogeny and Character Evolution Sinauer Associates Sunderland MA, USA
N. Molinero-Rosales M. Jamilena S. Zurita P. Gomez J. Capel R. Lozano (1999) ArticleTitleFALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity Plant J. 20 685–693
K.J. Niklas (1977) ArticleTitleApplication of finite element analysis to problems in plant morphology Ann. Bot. 41 133–153
N. Ori Y. Eshed G. Chuck J.L. Bowman S. Hake (2000) ArticleTitleMechanisms that control knox gene expression in the Arabidopsis shoot Development 127 5523–5532
A. Parnis O. Cohen T. Gutfinger D. Hareven D. Zamir E. Lifschitz (1997) ArticleTitleThe dominant developmental mutants of tomato, Mouse-ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene Plant Cell 9 2143–2158
V. Pautot J. Dockx O. Hamant. J. Kronenberger O. Grandjean D. Jublot J. Traas (2001) ArticleTitleKNAT2: Evidence for a link between knotted-like genes and carpel development Plant Cell 13 1719–1734
L. Reiser P. Sanchez-Baracaldo S. Hake (2000) ArticleTitleKnots in the family tree: evolutionary relationships and functions of knox homeobox genes Plant Mol. Biol. 42 151–166
R. Ruiz-Medrano B. Xoconostle-Cazarez W.J. Lucas (1999) ArticleTitlePhloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants Development 126 4405–4419
T. Sachs (1991) Pattern Formation in Plant Tissues Cambridge University Press New York
N. Sentoku Y. Sato N. Kurata Y. Ito H. Kitano M. Matsuoka (1999) ArticleTitleRegional expression of the rice KN1-type homeobox gene family during embryo, shoot, and flower development Plant Cell 11 1651–1664
L.G. Smith B. Greene B. Veit S. Hake (1992) ArticleTitleA dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates Development 116 21–30
Swofford, D.L., (2001). Phylogenetic Analysis using Parsimony (PAUP*. *and other methods), version 4. Sinauer Associates, Sunderland MA, USA
M. Tsiantis A. Hay (2003) ArticleTitleComparative plant development: the time of the leaf? Nature Rev. Genet. 4 169–180
R.W. Williams (1998) ArticleTitlePlant homeobox genes: many functions stem from a common motif BioEssays 20 280–282
S. Zachgo (2002) In situ Hybridization P.M. Gilmartin C. Bowler (Eds) Molecular Plant Biology EditionNumber2 Oxford University Press Oxford, UK 41–63
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The nucleotide sequence data reported will appear in the GenBank Nucleotide Sequence Database under the accession numbers DQ012434 (EcSTM), AY601274 (CmSTM), AY226559 (EcH4), AY594659 (CmH4).
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Groot, E.P., Sinha, N. & Gleissberg, S. 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 (2005). https://doi.org/10.1007/s11103-005-4548-1
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DOI: https://doi.org/10.1007/s11103-005-4548-1