Leaves in vascular plants are produced by determinate growth on the flanks of indeterminate shoot apical meristems. Inderminate growth of the shoot apical meristem is controlled by the knotted-like homeobox gene family (KNOX) (reviewed in Hake et al., 2004
). KNOX genes are present in some green algae (e.g. Acetabularia), mosses, ferns, gymnosperms and angiosperms and their function may be highly conserved (Sano et al., 2005). Over-expression of fern KNOX-like genes in Arabidopsis thaliana, for example, produces a similar phenotype (altered leaf shape) as over-expression of arabidopsis KNOX-like genes in Arabidopsis (Sano et al., 2005). Proper development of leaves requires permanent negative repression of KNOX genes and several genes have so far been discovered in euphyllophyte species for maintaining the KNOX-off state, including PHANTASTICA (PHAN) isolated from snapdragon (Antirrhinum majus) (Waites and Hudson, 1995) and homologues of PHAN in maize (Timmermans et al., 1999) and Arabidopsis (Byrne et al., 2000). The two sets of genes operate in a co-ordinated manner with KNOX-like transcription factors repressing determinate growth promoted by PHAN, and PHAN-like transcription factors repressing KNOX to promote indeterminacy.
The system is likely controlled by auxin, which determines the site of leaf initiation and is correlated with decreased KNOX and increased PHAN activity. Environmental influences on KNOX and PHAN are not known. However, it is interesting to note that the original PHAN mutation in Antirrhinum was temperature-sensitive so that plant morphology was approximately normal at 25 °C but altered at lower temperatures (Waites and Hudson, 1995), implying an interaction of PHAN-mediated morphogenesis with temperature-sensitive elements of leaf development. Genes such as PHAN may be prime candidates for involvement in the first stage of the telome theory, i.e. the evolution of determinant lateral shoot systems in trimerophytes (Fig. 1) (Cronk, 2001).
Leaf production also requires differentiation between adaxial (upper) and abaxial (lower) surfaces because the former is specialized for the efficient capture of solar energy and the latter for gas exchange. Deriving from the apical vegetative meristem flank, the abaxial surface is as old as land plants themselves, so genes specifying adaxial identity constitute a key innovation in leaf evolution (Cronk, 2001). Plants appear to have evolved a complex hierarchy of transcription factor activation and depression, with the HD-ZIP (homeodomain–leucine zipper) gene family promoting adaxial leaf surfaces and others promoting abaxial differentiation (Cronk, 2001). Interestingly, HD-ZIP gene expression is subject to a novel form of post-transcriptional regulation involving microRNAs found in bryophytes, lycopods, ferns and seed plants suggesting that it may be very ancient, dating back more than 400 Myr (Floyd and Bowman, 2004). Interactions between HD-ZIP gene and vascular tissue polarity have been demonstrated in Arabidopsis (Emery et al., 2003) and, since vascular tissue predates the leaf (Kenrick and Crane, 1997), this suggests that the same developmental unit was recruited for leaf polarity (Emery et al., 2003).
Whether megaphylls, which arose independently in four vascular plant lineages (ferns, sphenopsids, progymnosperms and seed plants) (Boyce and Knoll, 2002; Osborne et al., 2004a, b), recruited the same gene systems is open to investigation (Cronk, 2001). However, this does seem a possibility given that a common developmental mechanism for leaf production appears to have been recruited independently at least twice in the evolution of land plants (Harrison et al., 2005).
Current understanding of the genetic controls of stomatal formation in response to environment signals is limited, although it is clear that genetic modification more strongly alters the relationship between stomatal density and pore size, with attendant effects on leaf gas exchange, than short-term changes in environmental conditions (Hetherington and Woodward, 2003). Stomatal research on Arabidopsis has identified the HIC (high carbon dioxide) gene, which responds to CO2 and negatively regulates stomatal formation (Gray et al., 2000). HIC encodes a putative 3-ketoacyl coenzyme-A synthase, an enzyme involved in the synthesis of wax components found in the cuticle. Wax-deficient mutant plants show a 42 % increase in stomatal density with CO2 enrichment to 1000 ppm compared with that at 400 ppm CO2 (Gray et al., 2000). The possible involvement of the HIC gene (or similar) in mediating stomatal formation under different CO2 concentrations in other plant groups remains to be seen.
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