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Hou, H. Morphological Plasticity of Leaves. Encyclopedia. Available online: https://encyclopedia.pub/entry/9814 (accessed on 14 August 2024).
Hou H. Morphological Plasticity of Leaves. Encyclopedia. Available at: https://encyclopedia.pub/entry/9814. Accessed August 14, 2024.
Hou, Hongwei. "Morphological Plasticity of Leaves" Encyclopedia, https://encyclopedia.pub/entry/9814 (accessed August 14, 2024).
Hou, H. (2021, May 19). Morphological Plasticity of Leaves. In Encyclopedia. https://encyclopedia.pub/entry/9814
Hou, Hongwei. "Morphological Plasticity of Leaves." Encyclopedia. Web. 19 May, 2021.
Morphological Plasticity of Leaves
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This entry is adapted from the peer-reviewed paper 10.3390/ijms22020765

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.

environment leaf morphological plasticity phytohormones

1. Introduction

Leaves are key interfaces between plants and their surrounding environment, functioning to capture sunlight, synthesize photosynthate, exchange gasses, sense ambient changes, and regulate their growth under heterogeneous conditions [1][2][3]. In part because of their sessile lifestyle, plants possess efficient systems of morphological plasticity and acclimation to environmental changes. The diversity of leaf shape, vein pattern, stomata, and other parameters not only vary among plants that belong to different species (Figure 1A) but also within a single plant [4][5][6] (Figure 1B). It is well known that the same genotype is capable of developing different phenotypes, which is regarded as the coordination of phenotype, development, and environment [7][8]. For example, heteroblasty was described as the changes in leaf shape during growth development [9], while anisophylly is coupled with asymmetry and leaf phyllotaxis [10]. Some species have even evolved the ability to develop significantly different leaf types under heterogeneous conditions, a phenomenon called heterophylly [11][12][13]. Furthermore, heteroblasty indicates the juvenile-to-adult transition marked by morphological changes, and it emphasizes the developmental stage-related plasticity [14]. However, heterophylly is an extreme morphological plasticity, which is induced by environmental conditions [12][13]. This morphological plasticity provides good models for studying leaf development. However, the mechanisms related to how plants sense environmental changes and develop final leaf forms is still not elucidated.

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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/).

Given the rapid developments of plant functional genomics, many genes controlling leaf development have been studied, and the regulatory networks underlying these morphological processes have been well characterized [15]. Despite the fact that leaf development is related to genotype, the final shape is adjusted by environmental conditions, such as light, temperature, atmospheric carbon dioxide (CO2) concentrations, and submergence, to adapt to environmental variables [1][16]. The modulation of phytohormone signaling and distributions is a very effective strategy for quick environmental responses. Phytohormones are long-range molecular signals and have key functions in regulating plant growth and leaf development [11][17][18][19][20][21][22][23][24][25][26]. Thus, environmentally induced changes in hormone concentration, distribution, and/or sensitivity can promote coordinated developmental responses [27][28][29][30][31].

2. Environmental Sensing and Adaptation to Light and Temperature

Photosynthesis efficiency depends on the light capture of leaves. As a result, the balance of maximizing light capture and minimizing the harmful impact of high light is a coordinated developmental response. For example, plants prefer to develop broad leaves to maximize light capture, but if the sunlight is too harsh it may lead to overheating and cause harm to the plants [32][33]. In contrast, leaf development also responds to shade (a reduction in the red (660 nm) to far-red (730 nm), R/FR), which is called shade avoidance syndrome (SAS), showing petioles elongation, leaf upward bending, and leaf area decreasing [34][35] (Figure 2A). The upward movement of the leaves allows the plant to elevate the position of the foliage in order to maximize light capture [34][36]. Other aspects are also affected by light, such as leaf complexity, stomata density, and leaf thickness, which increased in the high light conditions [16][37][38][39]. In Rorippa aquatica (Brassicaceae), leaf complexity is dramatically increased in high light conditions [40]. In some other species, such as Nuphar lutea (Nymphaeaceae), Rumex palustris (Polygonaceae), and Hygrophila difformis (Acanthaceae), light change even induced the rearrangement of chloroplasts and altered the photosynthetic biochemistry to adapt the plant to aquatic conditions [41][42][43]. The photoperiod also significantly regulates leaf form. For example, short daylength induced submerged leaves, while long daylength induced terrestrial leaves of P. palustris and Ranunculus aquatilis (Ranunculaceae) [44][45].

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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.

Increasing surrounding temperature affects numerous developmental traits among plants, and the morphological changes that occur in plants in response to temperature changes are called thermomorphogenesis [46][47][48]. In order to adapt to high temperatures, plants developed elongated hypocotyls and petioles, as well as a decrease in leaf thickness and an increasing stomatal density [47][49][50]. These morphological responses are believed to cool plants and reduce the damage caused by sunlight through the upward bending of leaves [46][51][52]. Leaf dissection has for a long-time been thought to correlate with ambient temperature [5]. For example, plants growing in cold climates tend to develop serrated or deep-lobed leaves, while plants growing in warm conditions display shallow-lobed leaves [53][54][55][56][57]. To some degree, leaf dissection was used as an indicator for predicting paleoclimate [5][58]. The change in temperature of a single leaf of R. aquatica affects the epidermal cell size in developing leaves, and hence the morphology of the whole plant is affected [1][59]. In Ludwigia arcuata (Onagraceae), low temperature induced the elongation of epidermal cells and thus lead to the aquatic leaf form [60]. It was recently verified that pectin and cortical microtubules drive morphogenesis in plant epidermal cells [61][62], but how these epidermal changes are regulated by temperature is still unknown.

It was verified that auxin signal functions to connect temperature sensing with growth responses in hypocotyls [63][64]. In Arabidopsis thaliana, temperature changes can be sensed by the inactivation of photoreceptors such as phytochrome B (phyB), whose function in thermoregulation operates via the PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) for high temperature-induced hypocotyl elongation [65][66]. High temperature-activated PIF4 directly upregulates the expression of auxin biosynthesis genes (e.g., YUCCA8, TAA1, and CYB79B2), and as a result, the accumulated auxin induces hypocotyl elongation and leaf hyponasty [67][68]. High temperature also induced PIF4 expression by inactivating EARLY FLOWERING 3 (ELF3) that directly represses PIF4. In high temperature conditions, ELF3 binding to the PIF4 promoter is decreased, and thus PIF4 was activated for thermomorphogenesis [69][70]. Auxin could theoretically induce elongation growth; however, it was recently reported that the phytohormone brassinosteroid (BR) activates elongation growth downstream of auxin to act in themomorphogenesis [71][72].

Temperature and light signals are integrated into the PIF and the relevant genetic network, which controls auxin biosynthesis [67][73]. Photomorphogenesis and shade avoidance responses, including stem/hypocotyl elongation are mediated by PIF4 [74]. The stability of the PIF4 protein is regulated by light, and it is dephosphorylated and stable in the dark, while it is rapidly phosphorylated by phyB-mediated signaling and degradation upon red light irradiation [74]. Interestingly, although phyB and PIF4 antagonistically regulate photomorphogenesis and shade avoidance responses, they cooperatively promote stomatal development in response to high light [39]. Shade also induces the expression of gibberellic acid (GA) biosynthetic enzymes and leads to an accumulation of GA, which then promotes the degradation of DELLAs. It was found that DELLA directly interacts with PIF4 and prevents it from binding to target promoters [75][76]. Besides, the ethylene response also shows short hypocotyls, short roots, and an exaggerated apical hook [77]. PIF4 also promotes ethylene biosynthesis by activating the expression of ethylene biosynthesis genes (e.g., ACS2, 6, 8, and 9) and enhances ethylene signaling by activating the transcription factor ETHYLENE INSENSITIVE 3 (EIN3) [78][79].

Light and temperature are the most critical environmental factors for plant growth, and even a slight change can lead to disasters of plants [80][81]. We mentioned above that PIF4 may be a key element that functions in the light/temperature-dependent morphological plasticity and the crosstalk of phytohormones such as auxin, ethylene, and GA. Future studies based on these gene pathways and phytohormones will not only reveal novel mechanisms on the light and temperature response but will also have implications on crop improvement through use of these plastic strategies.

3. Environmental Sensing and Adaptation to Submergence

Under flooding or submerged conditions, plants find it difficult to obtain enough O2 for respiration. Terrestrial plants, such as A. thaliana and Solanum lycopersicum (tomato), which are intolerant to flooding, find that submerged conditions induce their leaves to turn pale and suppresses their plant growth [73][82]. Deepwater rice survive periodic flooding and consequent oxygen deficiency by activating an internode growth of stems to keep above the water [83] (Figure 2B). In other species such as R. palustris, elongated leaves and decreased thickness helps the plant to obtain a relatively increased gas exchange under submerged conditions [41]. In some aquatic, dimorphic types of plants, their submerged leaves are always thin, narrow, or dissected and contain fewer stomata, while aerial leaves are thick, broad, and entire, and have more stomata [12][40][84][85]. Although narrow or dissected leaves are less efficient at absorbing sunlight than those with wider blades, they can better withstand the destructive force of water flow and more efficiently incorporate CO2 and mineral nutrients than entire leaves [86][87][88].

ABA and ethylene are key regulators of drought and submerge response, separately. ABA was regarded as a stress hormone, which accumulates rapidly in response to drought/dehydration stress and plays a crucial role in stomatal closure, root growth, and the production of protective metabolites [20][89]. ABA levels in unstressed plants are low, but accumulated highly under reduced water potentials by the activation of key synthesis genes 9-cis-epoxycarotenoid dioxygenases (NCEDs) [90]. Upon perception of ABA, the ABA receptor pyrabactin resistance 1 (PYR1)-like protein PYL, regulatory components of the ABA receptor (RCAR) proteins, inhibit the activity of clade A protein phosphatase type 2C (PP2C) phosphatases, thus releasing the subclass III sucrose nonfermenting 1-related kinase 2 (SnRK2s, including SnRK2.2, SnRK2.3, and SnRK2.6) to phosphorylate downstream proteins [91][92]. The arabidopsis protein kinases SnRK2s function as central and positive regulators of the ABA signaling pathway and are involved in stomatal closure, osmotic stress responses, and have an evolutionarily conserved function on plant adaptation to the terrestrial environment [93][94][95].

Aquatic plants, such as rice, have evolved adaptive mechanisms to survive under submergence. When subjected to flooding, rice or deepwater rice accumulates high ethylene, which activates gibberellin biosynthesis gene SEMIDWARF 1 (SD1), promotes GA-dependent elongation, and results in an “escape” strategy to reestablish contact with the air [83]. Recent studies have found that the submergence-induced GA accumulation activates ACCELERATOR OF INTERNODE ELONGATION 1 (ACE1), which confers cells of the intercalary meristematic region with the competence for cell division, leading to internode elongation in the presence of GA. In contrast, high GA repressed DECELERATOR OF INTERNODE ELONGATION 1 (DEC1) suppresses internode elongation, whereas downregulation of DEC1 allows internode elongation [96]. Under submerged conditions, ethylene also induces the expression of two ethylene response factors (ERFs), SNORKEL1 (SK1) and SK2, to trigger remarkable internode elongation via GA [97]. However, the response may vary between species, as GA levels in Rumex acetosa remain unchanged, although ethylene increased during submergence [98]. For the submergence of terrestrial plants, such as A. thaliana, the limited gas diffusion causes passive ethylene accumulation, leading to ETHYLENE INSENSITIVE 2 (EIN2) and EIN3/EIN3-like 1 (EIL1)-dependent signaling and enhanced production of the nitric oxide (NO) scavenger PHYTOGLOBIN 1 (PGB1). The enhanced PGB1 levels lead to NO depletion, enhancing group VII ethylene response factor (ERFVII) stability [99]. The constitutively synthesized ERVIIs (e.g., RELATED TO APETALA 2.12 (RAP2.12), RAP2.2, and RAP2.3) redundantly act as the principal activators of many hypoxia adaptive genes and lead to flooding survival [43].

Phytohormone signals also play key roles in leaf development. For example, the recruitment of leaf founder cells in the shoot apical meristem (SAM) is mediated by the formation of a concentration maxima of auxin [100][101]. Altering the endogenous auxin levels and localization results in leaf simplification in a tomato plant, while downregulating auxin biosynthesis genes (e.g., YUCCA) was reported to inhibit organ initiation in many species such as Arabidopsis, maize, and petunia [102][103][104]. Cytokinin (CK) also plays an important role in SAM maintenance [105][106][107]. Overexpression of the CK biosynthesis genes in tomato leaves leads to the formation of highly compound leaves. However, exogenous application of CK causes minor leaf phenotypes in the tomato [108]. Increasing GA levels in tomatoes result in tall plants with larger and simpler leaves [109]. Interestingly, this GA response is not common, and in some species, GA has the opposite effect of inducing more compound leaves [110][111]. To better understand the relationship of phytohormones and leaf development, in the next section we will discuss the molecular mechanisms of leaf development.

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Hongwei Hou
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