Plants show leaf form alteration in response to changes in the surrounding environment, and this phenomenon is called heterophylly. Although heterophylly is seen across plant species, the regulatory mechanisms involved are largely unknown. Here, we investigated the mechanism underlying heterophylly in Rorippa aquatica (Brassicaceae), also known as North American lake cress. R. aquatica develops pinnately dissected leaves in submerged conditions, whereas it forms simple leaves with serrated margins in terrestrial conditions. We found that the expression levels of KNOTTED1-LIKE HOMEOBOX (KNOX1) orthologs changed in response to changes in the surrounding environment (e.g., change of ambient temperature; below or above water) and that the accumulation of gibberellin (GA), which is thought to be regulated by KNOX1 genes, also changed in the leaf primordia. We further demonstrated that exogenous GA affects the complexity of leaf form in this species. Moreover, RNA-seq revealed a relationship between light intensity and leaf form. These results suggest that regulation of GA level via KNOX1 genes is involved in regulating heterophylly in R. aquatica. The mechanism responsible for morphological diversification of leaf form among species may also govern the variation of leaf form within a species in response to environmental changes.
Leaf morphogenesis relies on adaxial/abaxial patterning and extensive growth. This study investigated the role of ANGUSTIFOLIA3 (AN3) from Arabidopsis thaliana in these processes. The an3 mutants produce narrower leaves that contain significantly fewer cells than the wild type. We examined the genetic interaction between an3 and asymmetric leaves2 (as2), which has a weak adaxial defect. The an3 as2 mutants developed trumpet-like leaves and accumulated transcripts of abaxially expressed genes at higher levels than an3 and as2. Gene expression analyses suggested that an3 altered the expression of a number of genes. Many of them were involved in metabolism, and several genes that promote adaxial identity cooperatively with as2 were down-regulated. Next, we performed detailed developmental analyses to examine the relationship between the narrow-leaf phenotype of an3 and leaf polarity. As a result, we showed that AN3 is required during a specific phase after an oblong shape is established in early leaf primordia. During this phase, the angle of the cell division plane relative to the longitudinal axis of the leaf primordium is more variable than in the earlier phase where transverse divisions were dominant in both the wild type and an3. Correlated with this dynamic change in cell division pattern, the leaf primordium became rounder. In an3, mitotic activity was reduced more rapidly than in the wild type, causing premature termination of the morphometric change. These results suggest that AN3 promotes cell proliferation during a specific developmental phase that is also required to correct abaxial/adaxial patterning in concert with AS2.
Plant species are known to respond to variations in environmental conditions. Many plant species have the ability to alter their leaf morphology in response to such changes. This phenomenon is termed heterophylly and is widespread among land plants. In some cases, heterophylly is thought to be an adaptive mechanism that allows plants to optimally respond to environmental heterogeneity. Recently, many research studies have investigated the occurrence of heterophylly in a wide variety of plants. Several studies have suggested that heterophylly in plants is regulated by phytohormones. Herein, we reviewed the existing knowledge on the relationship and role of phytohormones, especially abscisic acid, ethylene, gibberellins, and auxins (IAA), in regulating heterophylly and attempted to elucidate the mechanisms that regulate heterophylly.
Understanding the evolutionary path of transcription factors is essential for the elucidation of plant evolution. The CRC/DL subfamily of the YABBY gene family are functionally diverse, plant-specific, putative transcription factors. In Arabidopsis thaliana, CRABS CLAW (CRC) is expressed in the abaxial region of carpel primordia and in floral nectaries, where it regulates carpel morphology and nectary development. By contrast, in Oryza sativa, DROOPING LEAF (DL) is expressed in the entire carpel primordium and in the central undifferentiated cells of leaves, where it regulates carpel identity and midrib development. Recent studies suggest that abaxial expression and functional roles in the carpel are ancestral characters, although when and how neo-functionalizations occurred remains unclear. To elucidate the evolutionary processes of the CRC/DL subfamily, we examined in situ expression patterns of a CRC ortholog (AaDL) in Asparagus asparagoides (Asparagales). Like CRC in Arabidopsis thaliana, AaDL was clearly expressed in the abaxial region of the ovary wall. Expression was also detected in the phloem of leaves, but not in the septal nectary. Thus, expression in the entire carpel primordium might have been acquired after the divergence of Asparagus, with expression competence in the leaves acquired before the divergence of Asparagus in monocots. Our data indicate that the evolution of CRC/DL subfamily genes occurred in a stepwise manner.
Lake cress, Rorippa aquatica (Brassicaceae), is a semi-aquatic plant that exhibits a variety of leaf shapes, from simple leaves to highly branched compound leaves, depending on the environment. Leaf shape can vary within a single plant, suggesting that the variation can be explained by a simple model. In order to simulate the branched structure in the compound leaves of R. aquatica, we implemented reaction-diffusion (RD) patterning onto a theoretical framework that had been developed for serration distribution in the leaves of Arabidopsis thaliana, with the modification of the one-dimensional reaction-diffusion domain being deformed with the spatial periodicity of the RD pattern while expanding. This simple method using an iterative pattern could create regular and nested branching patterns. Subsequently, we verified the plausibility of our theoretical model by comparing it with the experimentally observed branching patterns. The results suggested that our model successfully predicted both the qualitative and quantitative aspects of the timing and positioning of branching in growing R. aquatica leaves.
The genus Asparagus is unusual in producing axillary, determinate organs called cladodes, which may take on either a flattened or cylindrical form. Here, we investigated the evolution of cladodes to elucidate the mechanisms at play in the diversification of shoot morphology. Our observations of Asparagus asparagoides, which has leaf-like cladodes, showed that its cladodes are anatomically and developmentally similar to leaves but differ in the adaxial/abaxial polarity of the vasculature. In addition to the expression of an ortholog of KNAT1, orthologous genes that are normally expressed in leaves, ASYMMETRIC LEAVES1 and HD-ZIPIII, were found to be expressed in cladode primordia in a leaf-like manner. The cylindrical cladodes of Asparagus officinalis showed largely similar expression patterns but showed evidence of being genetically abaxialized. These results provide evidence that cladodes are modified axillary shoots, suggest that the cooption of preexisting gene networks involved in leaf development transferred the leaf-like form to axillary shoots, and imply that altered expression of leaf polarity genes led to the evolution of cylindrical cladodes in the A. officinalis clade.
Summary:The leaves of some plant species are able to change their morphology in response to environmental conditions. This phenomenon is termed heterophylly. Various aquatic plants exhibit drastic changes in leaf shape in response to submerged aquatic conditions. Heterophyllic variation ranges from mere modification of leaf width to drastic alteration in the outline of leaves and is interpreted as an adaptation to aquatic habitats. Although this phenomenon is widely observed among angiosperms, there is limited information on the regulation of heterophyllic switch in leaf development. Here, we have reviewed existing knowledge on leaf development and heterophylly and have introduced Neobeckia aquatica as an emerging model to elucidate the mechanisms underlying heterophylly.
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