Mechanisms of the Morphological Plasticity Induced by Phytohormones and the Environment in Plants

Abstract

Plants adapt to environmental changes by regulating their development and growth. As an important interface between plants and their environment, leaf morphogenesis varies between species, populations, or even shows plasticity within individuals. Leaf growth is dependent on many environmental factors, such as light, temperature, and submergence. Phytohormones play key functions in leaf development and can act as molecular regulatory elements in response to environmental signals. In this review, we discuss the current knowledge on the effects of different environmental factors and phytohormone pathways on morphological plasticity and intend to summarize the advances in leaf development. In addition, we detail the molecular mechanisms of heterophylly, the representative of leaf plasticity, providing novel insights into phytohormones and the environmental adaptation in plants.

Keywords: environment; leaf; molecular mechanism; morphological plasticity; phytohormones.

Figure 1

The phylogeny and typical leaf shape among plant species. (A) The phylogeny and typical leaf shape among species from different orders. Red text indicates the order name. (B) Leaves from a heterophyllous plant (Hygrophila difformis) shifted from terrestrial to submerged conditions. Successive leaves are in phyllotactic order. Bar = 1 cm. All photos were taken by the camera (Canon EOS80D, Japan) and plant materials were collected from the Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences (Institute of Hydrobiology, Chinese Academy of Sciences). The phylogenetic tree was based on the online software “Phylomatic” (http://phylodiversity.net/phylomatic/).

Figure 2

Example of plant developmental responses to environmental changes. (A) Both shaded light and an increase in temperature induce the elongation of the petiole, a reduction of leaf area, and an upward movement of the leaves. ELF3 directly represses PIF4, and this repression was released in shade/high temperature conditions. PIF4 activates auxin synthesis by upregulating YUCCAs and activating ethylene synthesis by upregulating ACSs for thermomorphogenesis and shade avoidance syndrome (SAS). Shade/high temperature also induces high levels of gibberellic acid (GA) and the degradation of DELLAs, which therefore release PIF4 for binding to target promoters. (B) Deepwater rice activates stem elongation growth depending on the water level. Submerged conditions accumulate high ethylene and activate SD1 for GA synthesis. GA promotes stem elongation through the activation of ACE1 and repression of DEC1. Ethylene also induced EIN2/EIN3 signaling and thus enhanced PGB1 to improve ERFVII stability for flooding survival.

Figure 3

Genetic and hormonal factors that control leaf development. (A) Genetic and hormonal factors are controlling primordium development. Class-I KNOTTED-LIKE HOMEOBOX (KNOXI) proteins maintain high cytokinin (CK) levels and low GA levels in the shoot apical meristem (SAM). ARP maintains high GA level through repression of KNOXI. (B) Adaxial-abaxial polarity establishment in a developing leaf. HD-ZIPIII functions antagonistically to KANADI (KAN) and YABBY (YAB) acts downstream of KAN on the abaxial side. miR165/166 represses HD-ZIPIII, but ASYMMETRIC LEAVES 1 (AS1) and AS2 promote the expression of HD-ZIPIII on the adaxial side and repress miR165/166, KAN, and YAB. ta-siRNAs target miR165/166 and Auxin response factor 3/4 (ARF3/4) to restrict them to the abaxial side. (C) Proximal-distal polarity establishment in a developing leaf. KNOXI genes are expressed in the boundary region, and CUP-SHAPED COTYLEDONS (CUCs) have positive feedbacks with KNOXI. Blade on PETIOLE 1 (BOP1) and BOP2 are expressed in the proximal region to repress KNOXI directly, or indirectly by AS2. ARF3/4 also repress KNOXI to promote organogenesis at the shoot apex. (D) The switch from cell proliferation to differentiation follows a process that is promoted by the miR319-TCP module and repressed by the miR396-GRF module. PRESSED FLOWER (PRS) is also repressed by class II TCP and NGATHA (NGA), promoting cell proliferation in the leaf margin. (E) Common molecular pathways underpin both simple and compound leaf formation. PIN-FORMED 1 (PIN1) localization at the developing leaf is polar so that an auxin activity maximum is formed at the tip of both serration and leaflet. KNOXI are expressed in the rachis of the compound leaf, where they activate CUC expression at the distal boundary of the leaflet and promote polar localization of PIN1 in the leaflets. In turn, CUC activity maintains KNOXI expression in the rachis while auxin downregulates KNOXI expression for leaflet formation. CUC expression and auxin maxima promote the development of serrations. Yellow represents an auxin activity maximum, red the domain of CUC expression, and the blue color denotes the expression domain of KNOXI. Panel A, C, and D is based on [121] and B is based on [122]. Panel E is based on [123].

Figure 4

Molecular mechanisms of heterophylly. (A) The mechanism of heterophylly in R. aquatica. Complex leaves were induced by the upregulated KNOXI and thus induced repression of Ga20ox1 and downregulated GA, while simple leaves were induced by the downregulated KNOXI and thus induced upregulated Ga20ox1 and GA. KNOXI also induced the accumulation of CK by the regulation of ISOPENTENYLTRANSFERASE 7 (IPT7). (B) The mechanism of heterophylly in R. trichophyllus. Terrestrial conditions induced ABA accumulation and activates HD-ZIPIII-mediated STOMAGEN (STO) and VASCULAR-RELATED NAC-DOMAIN 7 (VND7) upregulation via ABI3, while submerged conditions induced ethylene accumulation and activate KAN-mediated STO and VND7 downregulation via EIN3. (C) The heterophylly of C. grandiflora was induced by the temperature, dependent on REDUCED COMPLEXITY (RCO). Red in (A–C) represents upregulated genes or accumulated phytohormones, and green in (A–C) represents downregulated genes or phytohormones.