Opinion
Megaphylls, microphylls and the evolution of leaf development

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Originally coined to emphasize morphological differences, ‘microphyll’ and ‘megaphyll’ became synonymous with the idea that vascular plant leaves are not homologous. Although it is now accepted that leaves evolved independently in several euphyllophyte lineages, ‘megaphyll’ has grown to reflect another type of homology, that of euphyllophyte leaf precursor structures. However, evidence from the fossil record and developmental pathways fails to indicate homology and suggests homoplasy of precursor structures. Thus, as I discuss here, ‘megaphyll’ should be abandoned because it perpetuates an unsupported idea of homology, leading to misconceptions that pervade plant biology thinking and can bias hypothesis and inference in developmental and phylogenetic studies. Alternative definitions are needed that are based on development and phylogeny for different independently evolved leaf types.

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The microphyll–megaphyll dichotomy

In vascular plant sporophytes, leaves are lateral appendages that share four defining features: vascularization, determinate growth, bilateral symmetry (adaxial–abaxial polarity; hereafter referred to as ad/abaxial polarity) and definite arrangement (phyllotaxis). Despite these shared characteristics, leaves are not homologous across all vascular plants. An early step toward the recognition of this situation [1] was the defining of a major dichotomy between microphylls, small and simple leaves,

Morphological inconsistencies and overlap in the microphyll–megaphyll dichotomy

Microphylls are defined as leaves of small size, with simple venation (one vein) and associated with steles that lack leaf gaps (protosteles). By contrast, megaphylls are defined as leaves of generally larger size, with complex venation and associated with leaf gaps in the stele [3]. However, each of these criteria has inconsistencies [4] that highlight the disconnection between phylogeny and current morphological definitions at the level of the microphyll–megaphyll divide.

First, the presence

Phylogenetic and developmental perspectives

Definitions based on morphology thus seem to create more confusion and overlap between the microphyll and megaphyll concepts instead of clarifying them. The validity of the two concepts needs to be verified against comparative developmental data, genetic developmental pathways controlling leaf development and plant phylogenies that illuminate the relationships between extant taxa and their closest leafless relatives in the fossil record. Leaf evolution was the earliest major plant biology

How many different ‘megaphylls’ are there?

Multiple lines of evidence indicate that leaves that have been categorized as megaphylls are fundamentally different from each other. Some are associated with eustelic stems, whereas others are borne on siphonostelic or protostelic stems. In seed plants the adaxial domain of leaves has a developmentally associated axillary meristem; such structures are missing from seed-free plants. Cell differentiation and tissue maturation progress exclusively acropetally in fern leaves, but in seed-plant

‘Megaphyll’ precursor structures

The origin of euphyllophyte leaves from systems of 3D-branching axes, long advocated by students of the fossil record, received support from cladistic studies that proposed that synapomorphies of the euphyllophyte clade include: (i) monopodial or pseudomonopodial branching; and (ii) small, pinnulelike vegetative branches [8]. The corollaries of these synapomorphies are the presence of a main axis with subordinated lateral branching systems and determinate growth of the lateral branching

Process homology and homoplasy

Process homology refers to common inheritance of developmental genetic pathways [18]. In terms of gene pathways, three major determinants of leaf development have been commonly considered in discussions of the evolution of shoot systems: (i) interactions between class 1 KNOX genes and ARP genes; (ii) class III homeodomain-leucine zipper (HD-Zip) genes and their interactions with KANADI genes and microRNAs 165 and 166; and (iii) YABBY genes and their interactions with class 1 KNOX genes and leaf

Conclusions and future perspectives

The classic concepts of microphyll and megaphyll pervade thinking on the evolution of leaf development. As such, they influence significantly the process of science in plant biology by contributing to the shaping of evolutionary hypotheses and to inferences of developmental studies. However, the two concepts, as currently defined, are equivocal, partially overlapping and inconsistent with current understanding of plant phylogeny. Most workers are aware of this situation when they agree that

Acknowledgements

I thank Gar Rothwell, Heather Sanders and two anonymous reviewers for their constructive critique, helpful comments and suggestions.

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