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In a review article published in the February, 2001 issue of Current Opinion in Plant Biology, Drs. Mary Byrne, Marja Timmermans, Caterine Kidner and Rob Martienssen at the Cold Spring Harbor Laboratory, New York, discuss the genetic interactions between the shoot apical meristem (SAM) and the developing leaf primordium which condition early leaf patterning. The authors describe various steps involved in leaf development and offer explanation on the occurrence of radial symmetrical leaves. They provide by example how in various natural mutants and transgenics, the leaf shape changes. Evidence is presented that, for differentiation of leaves, it is necessary that KNOX class genes are suppressed
Giving details, the authors describe that the first step in leaf development is recruitment of founder cells. The shape of the leaf determines whether the recruitment of founder cells will be confined to (a) a small group of cells from the border of the SAM as in dicots such as Arabidopsis or (b) the entire group around the periphery of the SAM, as illustrated by maize. In the latter, mutations in the duplicate factor NARROW SHEATH result in deletion of the leaf margin. This is because the mutant fails to recruit sufficient numbers of founder cells necessary for normal sheath formation. Besides narrow sheath, there are other mutations such as leafbladeless1 (lbl1) and rough sheath2 (RS2) which interfere with the recruitment of founder cells, thereby affecting axis specifications.
The authors provide many examples where mutations in any of the steps regulating leaf development cause abnormal leaf shapes. In the cold-sensitive mutant phantasia (phan) of Antirrhinum, the development of the leaf is seriously hampered; patches of abaxial tissue grow on the upper (adaxial) side of the leaf, being surrounded by ectopic lamina outgrowth. The authors support of what Waites and Hudson have proposed that combination of both abaxial and adaxial domains is necessary for the normal development of the leaf; and that the absence of one domain renders the leaf radial. In the dominant phabulosa (phb1d) mutant in Arabidopsis, dorsoventral patterning is disturbed resulting in the formation of additional axillary meristems around their base. Among other mutations, known to disrupt dorsoventral patterning, are: PINHEAD (PNH) also known as ZWILLE (ZLL), and ARGONAUTE (AGO). The two last mentioned mutants show a dosage dependent interaction, the double mutants displaying a severe loss of axis formation.
The authors quote results of an interesting experiment, in which tobacco plants, transformed with the polycomb genes of Drosophila, show leaf shape changes, similar to that recorded in as1(asymmetrical leaves), rs2 and phan mutants. It has also been shown that in Arabidopsis, the CURLY LEAF gene encodes a protein similar to Trithorax-group protein and that the gene involved regulates MADS-box genes without affecting those in homeobox. The authors also refer to the mode of functioning of PHAN family members which suppress certain KNOX-class genes. This suppression plays a role in the differentiation of leaf-founder cells from stem cells in the shoot apical meristem.
Leaf initiation and development in monocots and dicots are divergent and yet there is a good deal of similarity between the rs2 and as1 genes which regulate the phenotype in maize, Arabidopsis respectively.
The reviewers discuss the complexity of complex leaf formation. Development of a compound leaf in tomato is disrupted when there is a faulty expression of KNOX genes. As a result, there is a change in leaf shapes: tomato leaves become filamentous or repeatedly ramified. KNOX genes do not act in the species with simple leaves. It is also suggested that in shoot apical meristems (SAM), genes similar to PHAN (phantisca) influence the sympodial growth habit of tomato. LEAFY (LFY), the floral meristem identity gene, also plays a role in the development of compound leaves. LEAFY (LFY) gene in Arabidopsis is the pea homolog of UNIFOLIATA (UNI) and snapdragon homolog of FLORICAULA. When UNI mutates, compound pea leaves are modified to simple leaves. Mutation of another floral meristem identity gene, the UNUSUAL FLORAL ORGANS (UFO) in Arabidopsis converts its simples leaves into lobed ones.
It is necessary to silence KNOX genes for the normal development of leaves and two genes RS2 (rough sheath 2) and AS1(asymmetrical leaves) perform this task of silencing. It is suggested that the last mentioned two genes encode transcription factors essential to keep epigenetic states in place.
In conclusion, the reviewers speculate that cellular memory may act preserving the distinction between stem-and founder cells contributing to the specifications of leaf shape through interaction.