Advertisement
JOURNAL ARTICLES
The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves
E. Semiarti, Y. Ueno, H. Tsukaya, H. Iwakawa, C. Machida, Y. Machida
Development 2001 128: 1771-1783;

Summary

The asymmetric leaves2 (as2) mutant of Arabidopsis thaliana generated leaf lobes and leaflet-like structures from the petioles of leaves in a bilaterally asymmetric manner. Both the delayed formation of the primary vein and the asymmetric formation of secondary veins were apparent in leaf primordia of as2 plants. A distinct midvein, which is the thickest vein and is located in the longitudinal center of the leaf lamina of wild-type plants, was often rudimentary even in mature as2 leaves. However, several parallel veins of very similar thickness were evident in such leaves. The complexity of venation patterns in all leaf-like organs of as2 plants was reduced. The malformed veins were visible before the development of asymmetry of the leaf lamina and were maintained in mature as2 leaves. In vitro culture on phytohormone-free medium of leaf sections from as2 mutants and from the asymmetric leaves1 (as1) mutant, which has a phenotype similar to that of as2, revealed an elevated potential in both cases for regeneration of shoots from leaf cells. Analysis by the reverse transcription-polymerase chain reaction showed that transcripts of the KNAT1, KNAT2 and KNAT6 (a recently identified member of the class 1 knox family) genes accumulated in the leaves of both as2 and as1 plants but not of wild type. Transcripts of the STM gene also accumulated in as1 leaves. These findings suggest that, in leaves, the AS2 and AS1 genes repress the expression of these homeobox genes, which are thought to maintain the indeterminate cell state in the shoot apical meristem. Taken together, our results suggest that AS2 and AS1 might be involved in establishment of a prominent midvein and of networks of other veins as well as in the formation of the symmetric leaf lamina, which might be related to repression of class 1 knox homeobox genes in leaves.

Reference

    1. Banno H.,
    2. Hirano K.,
    3. Nakamura T.,
    4. Irie K.,
    5. Nomoto S.,
    6. Matsumoto K.,
    7. Machida Y.
    (1993) NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases. Mol. Cell Biol 13, 4745–4752
    OpenUrlAbstract/FREE Full Text
    1. Barton M. K.,
    2. Poethig R. S.
    (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development 119, 823–831
    OpenUrlAbstract/FREE Full Text
    1. Berná G.,
    2. Robles P.,
    3. Micol J. L.
    (1999) A mutational analysis of leaf morphogenesis in Arabidopsis thaliana. Genetics 152, 729–742
    OpenUrlAbstract/FREE Full Text
    1. Byrne M.,
    2. Barley R.,
    3. Curtis M.,
    4. Arroyo J. M.,
    5. Dunham M.,
    6. Hudson A.,
    7. Martienssen R.
    (2000) Asymmetric leaves mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967–971
    OpenUrlCrossRefPubMed
    1. Candela H.,
    2. Martinez-Laborda A.,
    3. Micol J. L.
    (1999) Venation pattern formation in Arabidopsis thaliana vegetative leaves. Dev. Biol 205, 205–216
    OpenUrlCrossRefPubMedWeb of Science
    1. Carland F. M.,
    2. McHale N. A.
    (1996) LOP1: a gene involved in auxin transport and vascular patterning in Arabidopsis. Development 122, 1811–1819
    OpenUrlAbstract
    1. Carland F. M.,
    2. Berg B. L.,
    3. FitzGerald J. N.,
    4. Jinamrnphongs S.,
    5. Nelson T.,
    6. Keith B.
    (1999) Genetic regulation of vascular tissue patterning in Arabidopsis. Plant Cell 11, 2123–2137
    OpenUrlAbstract/FREE Full Text
    1. Chuck G.,
    2. Lincoln C.,
    3. Hake S.
    (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8, 1277–1289
    OpenUrlAbstract/FREE Full Text
    1. Conway L. J.,
    2. Poethig R. S.
    (1997) Mutations of Arabidopsis thaliana that transform leaves into cotyledons. Proc. Natl. Acad. Sci. USA 94, 10209–10214
    OpenUrlAbstract/FREE Full Text
    1. Deyholos M. K.,
    2. Cordner G.,
    3. Beebe D.,
    4. Sieburth L. E.
    (2000) The SCARFACE gene is required for cotyledon and leaf vein patterning. Development 127, 3205–3213
    OpenUrlAbstract
    1. Fabri O. C.,
    2. Schäffner A. R.
    (1994) An Arabidopsis thaliana RFLP mapping set to localize mutations to chromosomal regions. Plant J 5, 149–156
    1. Hake S.,
    2. Vollbrecht E.,
    3. Freeling M.
    (1989) Cloning Knotted, the dominant morphological mutant in maize using Ds2 as a transposon tag. EMBO J 8, 15–22
    OpenUrlPubMedWeb of Science
    1. Hamada S.,
    2. Onouchi H.,
    3. Tanaka H.,
    4. Kudo M.,
    5. Liu Y.G.,
    6. Shibata D.,
    7. Machida C.,
    8. Machida Y.
    (2000) Mutations in the WUSCHEL gene of Arabidopsis thaliana result in the development of shoots without juvenile leaves. Plant J 24, 91–101
    OpenUrlCrossRefPubMedWeb of Science
    1. Hareven D.,
    2. Gutfinger T.,
    3. Parnis A.,
    4. Eshed Y.,
    5. Lifschitz E.
    (1996) The making of a compound leaf: Genetic manipulations of leaf architecture in tomato. Cell 84, 735–744
    OpenUrlCrossRefPubMedWeb of Science
    1. Hickey L. J.
    (1973) Classification of the architecture of dicotyledonous leaves. Am. J. Bot 60, 17–33
    1. Höfler J.,
    2. Turner L.,
    3. Hellens R.,
    4. Ambrose M.,
    5. Matthews P.,
    6. Michael A.,
    7. Ellis N.
    (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol 7, 581–587
    OpenUrlCrossRefPubMedWeb of Science
    1. Kerstetter R. A.,
    2. Poethig R. S.
    (1998) The specification of leaf identity during shoot development. Annu. Rev. Cell Dev. Biol 14, 373–398
    OpenUrlCrossRefPubMedWeb of Science
    1. Kim G.-T.,
    2. Tsukaya H.,
    3. Uchimiya H.
    (1998) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev 12, 2381–2391
    OpenUrlAbstract/FREE Full Text
    1. Kinsman E. A.,
    2. Pyke K. A.
    (1998) Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125, 1815–1822
    OpenUrlAbstract
    1. Koizumi K.,
    2. Sugiyama M.,
    3. Fukuda H.
    (2000) A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development 127, 3197–3204
    OpenUrlAbstract
    1. Laux T.,
    2. Mayer K. F. X.,
    3. Berger J.,
    4. Jurgens G.
    (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87–96
    OpenUrlAbstract
    1. Lieu S. M.,
    2. Sattler R.
    (1976) Leaf development in Begonia hispida var. cucullifera with special reference to vascular organization. Can. J. Bot 54, 2108–2121
    OpenUrl
    1. Lincoln C.,
    2. Long J.,
    3. Yamaguchi J.,
    4. Serikawa K.,
    5. Hake S.
    (1994) A 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
    OpenUrlAbstract/FREE Full Text
    1. Long J. A.,
    2. Moan E. I.,
    3. Medford J. I.,
    4. Barton M. K.
    (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69
    OpenUrlCrossRefPubMed
    1. Long J. A.,
    2. Barton M. K.
    (2000) Initiation of axillary and floral meristems in Arabidopsis. Dev. Biol 218, 341–353
    OpenUrlCrossRefPubMedWeb of Science
    1. Lynn K.,
    2. Fernandez A.,
    3. Aida M.,
    4. Sedbrook J.,
    5. Tasaka M.,
    6. Masson P.,
    7. Barton M. K.
    (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126, 469–481
    OpenUrlAbstract
    1. Machida C.,
    2. Onouchi H.,
    3. Koizumi J.,
    4. Hamada S.,
    5. Semiarti E.,
    6. Torikai S.,
    7. Machida Y.
    (1997) Characterization of the transposition pattern of the Ac transposable element in Arabidopsis thaliana usingendonuclease I- Sce I. Proc. Natl. Acad. Sci. USA 94, 8675–8680
    OpenUrlAbstract/FREE Full Text
    1. Mattsson J.,
    2. Sung Z. R.,
    3. Berleth T.
    (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126, 2979–2991
    OpenUrlAbstract
    1. Mayer K. F. X.,
    2. Schoof H.,
    3. Haecker A.,
    4. Lenhard M.,
    5. Jurgens G.,
    6. Laux T.
    (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815
    OpenUrlCrossRefPubMedWeb of Science
    1. Nakashima M.,
    2. Hirano K.,
    3. Nakashima S.,
    4. Banno H.,
    5. Nishihama R.,
    6. Machida Y.
    (1998) The expression pattern of the gene for NPK1 protein kinase related to mitogen-activated protein kinase kinase kinase(MAPKKK) in a tobacco plant: correlation with cell proliferation. Plant Cell Physiol 39, 690–700
    OpenUrlAbstract/FREE Full Text
    1. Nelson T.,
    2. Dengler N.
    (1997) Leaf vascular pattern formation. Plant Cell 9, 1121–1135
    OpenUrlFREE Full Text
    1. Nishimura A.,
    2. Tamaoki M.,
    3. Sakamoto T.,
    4. Matsuoka M.
    (2000) Over-expression of tobacco knotted −1-type class1 homeobox genes alters various leaf morphology. Plant Cell Physiol 41, 583–590
    1. Okada K.,
    2. Ueda J.,
    3. Komaki M. K.,
    4. Bell C. J.,
    5. Shimura Y.
    (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3, 677–684
    OpenUrlAbstract/FREE Full Text
    1. Onouchi H.,
    2. Nishihama R.,
    3. Kudo M.,
    4. Machida Y.,
    5. Machida C.
    (1995) Visualization of site-specific recombination catalyzed by a recombinase from Zygosaccharomyces rouxii in Arabidopsis thaliana. Mol. Gen. Genet 247, 653–660
    OpenUrlCrossRefPubMedWeb of Science
    1. Ori N.,
    2. Eshed Y.,
    3. Chuck G.,
    4. Bowman J. L.,
    5. Hake S.
    (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127, 5523–5532
    OpenUrlAbstract
    1. Parnis A.,
    2. Cohen O.,
    3. Gutfinger T.,
    4. Hareven D.,
    5. Zamir D.,
    6. Lifschitz E.
    (1997) The 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
    OpenUrlAbstract/FREE Full Text
    1. Poethig R. S.
    (1997) Leaf morphogenesis in flowering plants. Plant Cell 9, 1077–1087
    OpenUrlFREE Full Text
    1. Przemeck G. K.,
    2. Mattsson J.,
    3. Hardtke C. S.,
    4. Sung Z. R.,
    5. Berleth T.
    (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200, 229–237
    OpenUrlPubMedWeb of Science
    1. Schneeberger R.,
    2. Tsiantis M.,
    3. Freeling M.,
    4. Langdale J. A.
    (1998) The ROUGH SHEATH2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125, 2857–2865
    OpenUrlAbstract
    1. Serikawa K. A.,
    2. Zambryski P. C.
    (1997) Domain exchanges between KNAT3 and KNAT1 suggest specificity of the kn1-like homeodomains requires sequences outside of the third helix and N-terminal arm of the homeodomain. Plant J 4, 863–869
    1. Serrano-Cartagena J.,
    2. Robles P.,
    3. Ponce M. R.,
    4. Micol J. L.
    (1999) Genetic analysis of leaf form mutants from the Arabidopsis Information Service collection. Mol. Gen. Genet 261, 725–739
    OpenUrlCrossRefPubMedWeb of Science
    1. Siegfried K. R.,
    2. Eshed Y.,
    3. Baum S. F.,
    4. Otsuga D.,
    5. Drews G. N.,
    6. Bowman J. L.
    (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117–4128
    OpenUrlAbstract
    1. Sinha N. R.,
    2. Williams R. E.,
    3. Hake S.
    (1993) Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7, 787–795
    OpenUrlAbstract/FREE Full Text
    1. Timmermans M. C. P.,
    2. Hudson A.,
    3. Becraft P. W.,
    4. Nelson T.
    (1999) ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284, 151–153
    OpenUrlAbstract/FREE Full Text
    1. Tsiantis M.,
    2. Schneeberger R.,
    3. Golz J. F.,
    4. Freeling M.,
    5. Langdale J. A.
    (1999) The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284, 154–156
    OpenUrlAbstract/FREE Full Text
    1. Tsukaya H.,
    2. Uchimiya H.
    (1997) Genetic analyses of the formation of the serrated margin of leaf blades in Arabidopsis: combination of a mutational analysis of leaf morphogenesis with the characterization of a specific marker gene expressed in hydathodes and stipules. Mol. Gen. Genet 256, 231–238
    OpenUrlCrossRefPubMedWeb of Science
    1. Waites R.,
    2. Selvadurai H. R. N.,
    3. Oliver I. R.,
    4. Hudson A.
    (1998) The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93, 779–789
    OpenUrlCrossRefPubMedWeb of Science
    1. Whaley W. G.,
    2. Whaley C. Y.
    (1942) A developmental analysis of inherited leaf patterns in Tropaeolum. Am. J. Bot 29, 105–194
    OpenUrlCrossRef
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves
E. Semiarti, Y. Ueno, H. Tsukaya, H. Iwakawa, C. Machida, Y. Machida
Development 2001 128: 1771-1783;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights