Temporal regulation of vegetative phase change in plants

Abstract

During their vegetative growth, plants reiteratively produce leaves, buds, and internodes at the apical end of the shoot. The identity of these organs changes as the shoot develops. Some traits change gradually, but others change in a coordinated fashion, allowing shoot development to be divided into discrete juvenile and adult phases. The transition between these phases is called vegetative phase change. Historically, vegetative phase change has been studied because it is thought to be associated with an increase in reproductive competence. However, this is not true for all species; indeed, heterochronic variation in the timing of vegetative phase change and flowering has made important contributions to plant evolution. In this review, we describe the molecular mechanism of vegetative phase change, how the timing of this process is controlled by endogenous and environmental factors, and its ecological and evolutionary significance.

Keywords: Arabidopsis; SPL genes; developmental timing; flowering time; heterochrony; leaf development; maize; miR156; miR172; shoot development; vegetative phase change.

Figure 1:. Species-specific patterns of vegetative phase change

A) Acacia saligna is typical of over 1,000 species of Acacia in Australia. These species initially produce compound leaves, and then produce leaves with a vertically expanded base and a compound tip before finally producing a simple, vertically oriented leaf known as a phyllode. B) Vachellia collinsii initially produces compound leaves with a small extra floral nectary (EFN) on the petiole and small stipules. At the 5–10^th node, it begins to produce leaves with a large EFN, large thorn-like stipules, and Beltian Bodies (BB) on the tips of leaflets. The juvenile leaves of this plant have abscised, but their small stipules are still visible. C) Juvenile and adult leaves in maize are distinguished by a variety of epidermal traits including the presence or absence of epidermal hairs and bulliform cells, the staining of the cell wall with Toluidine blue, cuticle thickness, and the shape of the lateral and outer cell walls of pavement cells. D) Rosette leaves of the Columbia accession of Arabidopsis grown under long day conditions. As described in the text, the morphology of these leaves and the distribution of abaxial trichomes (shown schematically as white marks) allows shoot development to be divided into the 4 phases shown here.

Figure 2:. miR156 is expressed in a similar pattern in a short-lived annual and in a perennial tree.

A) The relative level of miR156 in successive rosette leaves of Arabidopsis plants (Columbia) grown in short days to delay flowering. Modified with permission from Fig. 2 in He et al. B) The relative level of miR156 in successive leaves of seed-grown plants of the aspen Populus tremula x alba. A cross section of the petiole is shown below the leaf blade to illustrate its change in shape (round to eliptical) and vascular pattern. Modified with permission from Fig. 1 in Lawrence et al. C) Arabidopsis plant transformed with a genomic SPL9-GUS construct. There is no visible GUS activity in the cotyledons (C) and in leaves 1&2, consistent with the very high level of miR156 in these organs. GUS activity increases in successive leaves starting with leaf 3. Modified with permission from Fig. 2 in Xu et al.

Figure 3:. The mechanisms by which phase-specific traits are regulated by miR156/miR157.

Active genes/functions are represented by black lines and black text, and inactive genes and functions are represented by gray lines and text. The result of these genetic interactions is provided at the bottom of the figure.

Figure 4:. Model for the epigenetic regulation of MIR156 transcription in Arabidopsis.

This model combines data from studies of MIR156A and MIR156C, which are regulated by slightly different epigenetic mechanisms that have not been completely elucidated. MIR156 transcription is regulated by nucleosome remodeling and histone modifications. During the juvenile phase, the chromatin remodeler, Brahma (BRM), repositions the +2 and −1 nucleosome to promote transcription, while PKL prevents repositioning of the +1 nucleosome. It is unclear whether BRM remains at MIR156 genes during the adult phase, but in any case, PKL appears to have a more significant effect at this stage. PKL represses transcription both by inhibiting nucleosome repositioning and through its association with histone deacetylases, most importantly, HDA9. The loss of the active mark, H3K27ac, is associated with an increase in the repressive mark, H3K27me3, which is deposited by PRC2. Binding of PRC2 to MIR156 is promoted by PRC1 but can also occur independently of PRC1. In addition to promoting the activity of PRC2, PRC1 may represses MIR156 transcription via H2A ubiquitination. The transcription factor, VAL1, is present at MIR156 throughout development and binds to the BMI1A component of PRC1, facilitating its association with MIR156. However, VAL1 is not responsible for the temporal regulation of PRC1 or PRC2 activity.