Genetic Control of Leaf Shape

Abstract

The variability in leaf morphology is vast; therefore, an understanding of how leaves achieve this diversity has captured the attention of many developmental biologists. Genetic mechanisms that regulate leaf shape are repeated throughout both development and between species. Leaves initiate off the shoot apical meristem and development proceeds from cell division to cell elongation. Leaf initiation and the establishment of the three main axes of a leaf are largely directed by the plant hormone auxin. Work across species reveals that adjustments to the repeated interaction of auxin, gene expression changes and small ribonucleic acid (RNA) regulation allowed species‐specific leaf shape differences to emerge. Further, genetic interactions leading to patterning in simple leaf development are reiterated during establishment of leaf complexity. To understand leaf development in an evolutionary context, future research must take advantage of the ever‐expanding genomic tools in nonmodel organisms that exhibit leaf shape diversity.

Key Concepts:

  • Leaves originate from clusters of stem cells called meristems.

  • The development of leaves occurs along three main axes: (1) adaxial/abaxial, (2) proximal/distal and (3) medial/lateral.

  • The development of both meristems and leaves involve morphogenetic activity in zones which are defined by distinct gene expression and cell division/elongation patterns.

  • The transport and concentration of the hormone auxin largely directs many aspects of leaf morphogenesis.

  • Leaf and leaflet initiation first begin with the formation of auxin maxima.

  • Recycling of genetic mechanisms is a theme that occurs throughout leaf development.

Keywords: abaxial; adaxial; HDZIPIII ; KANADI ; leaf; marginal blastozone; miRNA; polarity; PIN‐FORMED ; YABBY

Figure 1.

Leaf development zones and cell division patterns. (a) Schematic of a shoot displaying the three major leaf axes and location of meristems (grey). (b) Three domains of the meristem: central zone (CZ, pink), peripheral zone (PZ, green) and rib zone (RZ, orange). Schematic of meristem domains, L1 (grey), L2 (blue), L3 (yellow). The first leaf to initiate is Primordia 1(P1), second is P2 and the site of the next leaf initiation is I1 (dotted circle). (c) Only anticlinal cell divisions (red dotted line) occur on the L1 and L2 layers, both types anticlinal and periclinal (purple dotted line) occur in L3. (d) Gradients of cell division to differentiation from primary morphogenesis (1° Morph) (dark blue) to 2° Morph (white) on a dicot leaf (simple and complex) and on a monocot leaf (maize); * indicates leaflets on a complex leaf.

Figure 2.

Gene expression and auxin patterning on apices of a species making complex leaves. (a) and (b) Schematic of the gene expression of KNOX1 (yellow hatched) and CUC/NAM (red). Auxin concentration and auxin transport pathways (blue), darker shade shows higher auxin concentration and lighter lower auxin concentration. (c) and (d) Auxin localisation patterns from auxin‐responsive reporter, DR5::Venus (Heisler et al., ) in tomato on the (c) adaxial side of a P4 leaf and an (d) apex containing I1, P1 and P2.

Figure 3.

Adaxial and abaxial identity at the cellular level in most species and on radialised leaf structures. (a) Schematic of a cross‐section through a mature dicot leaf. Adaxial tissues, adaxial epidermis (dE) and palisade mesophyll (PM), are light blue and xylem (Xy, blue) is present on the adaxial side of a vascular bundle. Abaxial tissue structures, abaxial epidermis (bE) and spongy mesophyll (SM), are pink and the abaxial side of the vascular bundle is the phloem (Ph, red). (b) In many dicot species, the defining characteristic of the central vascular bundle in a leaf is Xy in the adaxial position and Ph in the abaxial position. Leaves that have completely lost abaxial identity are radial (no blade outgrowth) and have a central vascular bundle consisting of only Xy surrounded by adaxial tissue. Leaves with complete loss of adaxial identity are radial and only Ph surrounded by abaxial tissue.

Figure 4.

Genetic regulation of abaxial and adaxial cell fate determination and maintenance. (a) Adaxially localised HD‐ZIPIIIs (REV, PHV and PHB) have an indirect (dotted lines) antagonistic relationship with abaxial localised KANDI genes. REV, PHV, PHB are further downregulated by the abaxial localised miR165/6. KANADI gene also has a direct (solid line) antagonistic relationship with AS2 which interacts with AS1 to form a protein complex. (b) miR390, along with AGO7, TAS3 and SGS3, is required for ta‐siARF biogenesis. ta‐siARFs directly repress ARF3 (an abaxial determinant) in the adaxial domain. (c) ta‐siARFs biogenesis is localised to the adaxial side by adaxial localisation of ta‐siARF biogenesis components TAS3 (orange) and AGO7 (red) in Arabidopsis and miR390 in maize.

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Further Reading

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Martinez, Ciera C, and Sinha, Neelima R(Sep 2013) Genetic Control of Leaf Shape. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020101.pub2]