Simple and Divided Leaves in Ferns: Exploring the Genetic Basis for Leaf Morphology Differences in the Genus Elaphoglossum (Dryopteridaceae)

Abstract

Despite the implications leaves have for life, their origin and development remain debated. Analyses across ferns and seed plants are fundamental to address the conservation or independent origins of megaphyllous leaf developmental mechanisms. Class I KNOX expression studies have been used to understand leaf development and, in ferns, have only been conducted in species with divided leaves. We performed expression analyses of the Class I KNOX and Histone H4 genes throughout the development of leaf primordia in two simple-leaved and one divided-leaved fern taxa. We found Class I KNOX are expressed (1) throughout young and early developing leaves of simple and divided-leaved ferns, (2) later into leaf development of divided-leaved species compared to simple-leaved species, and (3) at the leaf primordium apex and margins. H4 expression is similar in young leaf primordia of simple and divided leaves. Persistent Class I KNOX expression at the margins of divided leaf primordia compared with simple leaf primordia indicates that temporal and spatial patterns of Class I KNOX expression correlate with different fern leaf morphologies. However, our results also indicate that Class I KNOX expression alone is not sufficient to promote divided leaf development in ferns. Class I KNOX patterns of expression in fern leaves support the conservation of an independently recruited developmental mechanism for leaf dissection in megaphylls, the shoot-like nature of fern leaves compared with seed plant leaves, and the critical role marginal meristems play in fern leaf development.

YABBY Genes in the Development and Evolution of Land Plants

“…The emergence of leaves, which occurred shortly after plants had conquered the land, became one of the most important events both in the evolution of plants and in the ecology of the Earth. However, the evolutionary origin of leaves is still under discussion [ 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 ]. Different viewpoints can be summarised into three scenarios based primarily on paleobotanical, morphological, and anatomical data: (1) the leaves of all plants share a common origin and are homologous to the system of the leafless axes, or telomes, of the first terrestrial plants (Rhyniophyta sensu lato ), and their morphological differences in different taxa result from reduction or elaboration of these telome systems [ 3 , 4 ]; (2) while the leaves of most plants (called telome leaves, or megaphylls) indeed arose as a result of modification of the telome system, the leaves of some plants (at least of the lycophytes) that are termed enations or microphylls originated de novo as outgrowths of the cortex and epidermis of leafless telomes; therefore, there were two independent origins of plant leaves in evolution [ 1 ]; (3) leaves in different plant taxa originated independently more than two times through various mechanisms; the sterilisation of sporangia among them [ 2 , 5 , 6 , 8 ].…”

“…and its presence was implied in Osmunda regalis [ 7 , 8 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 ]. However, the hypotheses based on few studies that report the expression patterns of the above genes support different scenarios of leaf origin [ 7 , 25 , 26 , 28 , 34 , 35 ]. The presence of both KNOX and ARP homologues in the shoot tips of both lycophytes with microphylls and ferns with megaphylls has been interpreted as an indication of similar molecular regulation of organogenesis in these plant taxa and hence of a common evolutionary origin of leaves in all land plants [ 28 ].…”

EvoDevo: Past and Future of Continuum and Process Plant Morphology

“…However, surgical or chemical treatment may change the developmental fate of what was supposed to become a leaf. In some ferns at least (e.g., species of Dryopteris, Hypolepis, Osmunda), such experimentally induced changes include the developmental switch from a leaf (frond) primordium to a shoot (rhizome) bud and vice versa [176,177].…”

“…New EvoDevo studies on ferns point to the remarkable similarity of compound leaves (fronds) and shoots [72,104,177]. Raphael Cruz et al [72] (p. 2) wrote: "Fern leaves are different from most seed plant leaves.…”

“…Their conclusion: "Fern apical meristems should be interpreted as a complex and highly organized interconnected network of cells with indeterminate fates, specialized zones (apical cells vs. peripheral cells), and the capacity for producing new organs (leaves or pinnae)." According to Cruz et al [72,104], Harrison and Morris [60], Harrison et al [148], Plackett et al [109], and Vasco and Ambrose [177] fern leaves and their segments have to be interpreted evolutionarily and ontogenetically as reduced shoots. Thus, the presence of shoot-like features in developing leaves is strong evidence in favor of Agnes Arber's partial shoot theory (see Section 3.4).…”