What determines a leaf's shape?

Abstract

The independent origin and evolution of leaves as small, simple microphylls or larger, more complex megaphylls in plants has shaped and influenced the natural composition of the environment. Significant contributions have come from megaphyllous leaves, characterized usually as flat, thin lamina entrenched with photosynthetic organelles and stomata, which serve as the basis of primary productivity. During the course of evolution, the megaphylls have attained complexity not only in size or venation patterns but also in shape. This has fascinated scientists worldwide, and research has progressed tremendously in understanding the concept of leaf shape determination. Here, we review these studies and discuss the various factors that contributed towards shaping the leaf; initiated as a small bulge on the periphery of the shoot apical meristem (SAM) followed by asymmetric outgrowth, expansion and maturation until final shape is achieved. We found that the underlying factors governing these processes are inherently genetic: PIN1 and KNOX1 are indicators of leaf initiation, HD-ZIPIII, KANADI, and YABBY specify leaf outgrowth while ANGUSTIFOLIA3 and GROWTH-REGULATING FACTOR5 control leaf expansion and maturation; besides, recent research has identified new players such as APUM23, known to specify leaf polarity. In addition to genetic control, environmental factors also play an important role during the final adjustment of leaf shape. This immense amount of information available will serve as the basis for studying and understanding innovative leaf morphologies viz. the pitchers of the carnivorous plant Nepenthes which have evolved to provide additional support to the plant survival in its nutrient-deficient habitat. In hindsight, formation of the pitcher tube in Nepenthes might involve the recruitment of similar genetic mechanisms that occur during sympetaly in Petunia.

Keywords: Auxin; Environmental factors; Leaf shape; Morphological novelty; Nepenthes; Polarity specification.

Figure 1

Diversity in leaf forms across land plants. (A) Selected representatives of the different types of leaf forms found in non-vascular and vascular model plant species viz. Physcomitrella patens (non-vascular), Selaginella kraussiana (microphyll), Arabidopsis thaliana (simple megaphyll), and Solanum lycopersicum (compound megaphyll). (B) Selected representatives of uncommon and innovative leaf morphology found in vascular non-model plant species viz. Christia obcordata (butterfly-shaped leaf), Nepenthes khasiana, and Monstera deliciosa (modified leaf). Contributors of photographs used in the figure can be found in the Acknowledgements section.

Figure 2

Diagram illustrating stages of leaf initiation in selected model plant species viz. (A) Arabidopsis thaliana; (B) caulescent Streptocarpus sp. (simple leaf eudicots); (C) Solanum lycopersicum (compound leaf eudicot); (D) Zea mays (simple leaf monocot); and (E) Selaginella kraussiana (microphyll). Black arrowhead indicates PIN1 polarization; white arrowhead denotes auxin maxima; blue arrow shows the direction of auxin flow; black arrow represents upregulation; blunt end indicates repression; red arrow depicts downregulation; yellow dots represent auxin; square bracket indicates leaf founder cells recruitment sites. Illustrations are adapted from Byrne et al. [31] for A. thaliana; Nishii et al. [84] for Streptocarpus sp. (caulescent); Koltai and Bird [85] for S. lycopersicum; Timmermans et al. [33] and Tsiantis et al. [32] for Z. mays; Harrison et al. [20] and Sanders and Langdale [83] for S. kraussiana. L1, L2 = tunica; L3 = corpus.

Figure 3

Diagram illustrating leaf outgrowth in Arabidopsis. (A) Leaf primordium initiation; (B) leaf outgrowth; (C) adaxial/abaxial patterning (magnified view of inlet in B depicts the underlying genetic mechanisms controlling adaxial/abaxial patterning); (D) medial/lateral patterning (magnified view of inlet in B shows the underlying genetic mechanisms controlling mediolateral patterning). Illustrations are adapted from references mentioned in the text. P₁: plastochron 1; P₂: plastochron 2; I₁: incipient site showing auxin maxima (yellow circle). Pro/dis: proximal/distal; med/lat: medial/lateral; ad/ab: adaxial/abaxial.

Figure 4

Diagram illustrating leaf margin development in Arabidopsis. Magnified view of inlet shows the underlying genetic mechanisms controlling this process. Illustrations are adapted from Nikovics et al. [61], Bilsborough et al. [141], and Engelhorn et al. [63]. P₁: plastochron 1; P₂: plastochron 2; I₁: incipient site showing auxin maxima (yellow circle).