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Water-Wisteria as an ideal plant to study heterophylly in higher aquatic plants

DOI:10.1007/s00299-017-2148-6
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Gaojie Li
Gaojie Li
Gaojie Li
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Shiqi Hu
Shiqi Hu
Shiqi Hu
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Jingjing Yang
Jingjing Yang
Jingjing Yang
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Elizabeth A Schultz at University of Lethbridge
Elizabeth A Schultz
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Abstract and Figures

Key message: The semi-aquatic plant Water-Wisteria is suggested as a new model to study heterophylly due to its many advantages and typical leaf phenotypic plasticity in response to environmental factors and phytohormones. Water-Wisteria, Hygrophila difformis (Acanthaceae), is a fast growing semi-aquatic plant that exhibits a variety of leaf shapes, from simple leaves to highly branched compound leaves, depending on the environment. The phenomenon by which leaves change their morphology in response to environmental conditions is called heterophylly. In order to investigate the characteristics of heterophylly, we assessed the morphology and anatomy of Hygrophila difformis in different conditions. Subsequently, we verified that phytohormones and environmental factors can induce heterophylly and found that Hygrophila difformis is easily propagated vegetatively through either leaf cuttings or callus induction, and the callus can be easily transformed by Agrobacterium tumefaciens. These results suggested that Hygrophila difformis is a good model plant to study heterophylly in higher aquatic plants.
Leaf morphology and developmental stages of H. difformis leaves grown under different conditions. a A plant grown in terrestrial environments. b A plant grown in submerged environments. c Terrestrial leaf (left) and submerged leaf (right). d–h Leaves from a plant shifted from terrestrial to submerged conditions. Successive leaves are in phyllotactic order. d A fully terrestrial leaf; e–g Three successive transitional leaves; h A fully aquatic leaf. Black arrowheads indicates where leaflets, typical of the submerged form, are initiated. Note that the aquatic form is acquired initially at the base and shifts toward the apex in successive leaves. i–m Leaves from a plant shifted from submerged to terrestrial conditions. Successive leaves are in phyllotactic order. i A fully submerged leaf, j–l Three successive transitional leaves, m A fully terrestrial leaf. Note that successive leaves are increasingly less dissected. n–o The shoot apex of a plant grown under terrestrial conditions (left) and submerged conditions (right) with surrounding leaf primordia (P3). p–s Analysis of serration initiation from a plant grown under terrestrial conditions. Serrations are labeled with numbers reflecting their basipetal order of initiation. White arrowhead indicates a newly emerged serration. t–w Analysis of leaflet initiation from a plant grown under submerged conditions. Leaflets are labeled with numbers reflecting their basipetal order of initiation. White arrowheads indicate newly emerged leaflets. x Dissection index (DI) of successive leaves (P10 to P6) from plants shifted to different conditions. Data are mean ± SD (n = 5). The DI increases when terrestrial plants are shifted to submerged conditions whereas DI decreases when submerged plants are shifted to terrestrial conditions. Bars 1 cm in a–m and bars 1 mm in n–w
Leaf morphology and developmental stages of H. difformis leaves grown under different conditions. a A plant grown in terrestrial environments. b A plant grown in submerged environments. c Terrestrial leaf (left) and submerged leaf (right). d–h Leaves from a plant shifted from terrestrial to submerged conditions. Successive leaves are in phyllotactic order. d A fully terrestrial leaf; e–g Three successive transitional leaves; h A fully aquatic leaf. Black arrowheads indicates where leaflets, typical of the submerged form, are initiated. Note that the aquatic form is acquired initially at the base and shifts toward the apex in successive leaves. i–m Leaves from a plant shifted from submerged to terrestrial conditions. Successive leaves are in phyllotactic order. i A fully submerged leaf, j–l Three successive transitional leaves, m A fully terrestrial leaf. Note that successive leaves are increasingly less dissected. n–o The shoot apex of a plant grown under terrestrial conditions (left) and submerged conditions (right) with surrounding leaf primordia (P3). p–s Analysis of serration initiation from a plant grown under terrestrial conditions. Serrations are labeled with numbers reflecting their basipetal order of initiation. White arrowhead indicates a newly emerged serration. t–w Analysis of leaflet initiation from a plant grown under submerged conditions. Leaflets are labeled with numbers reflecting their basipetal order of initiation. White arrowheads indicate newly emerged leaflets. x Dissection index (DI) of successive leaves (P10 to P6) from plants shifted to different conditions. Data are mean ± SD (n = 5). The DI increases when terrestrial plants are shifted to submerged conditions whereas DI decreases when submerged plants are shifted to terrestrial conditions. Bars 1 cm in a–m and bars 1 mm in n–w
… 
Leaf morphological and anatomical characters of H. difformis.a Scanning electron micrographs of the abaxial side of a terrestrial leaf. Black circle indicates glandular trichome, white circle indicates nonglandular trichome. b Stomas and epidermal cells of the adaxial side of a terrestrial leaf. c Stomas and epidermal cells of the abaxial side of a terrestrial leaf. d Scanning electron micrographs of the abaxial side of a submerged leaf. Black circle shows glandular trichome. Note that only glandular trichomes grow on the submerged leaf lamina and midvein, and these trichomes are shorter than those on the terrestrial leaf. e Stomas and epidermal cells of the adaxial side of a submerged leaf. Note that epidermal cells of submerged leaves are smaller and have more lobes resulting in a more pronounced jigsaw shape. f Stomas and epidermal cells of the abaxial side of a submerged leaf. g Comparison of stomatal density: the number of stoma on both sides per unit area. Measured areas were 0.15 mm². Data are mean ± SD (n = 10). Bars marked with letters a, b or c are statistically different according to the Student’s t test (P < 0.05). h Cross sections of terrestrial leaf and its semithin section (i). Note that terrestrial leaves are thick and have obvious differentiation of palisade tissue and spongy tissue (j), cross sections of terrestrial leaf vascular bundle and its magnification (k). l Cross sections of submerged leaf and its semithin section (m). Note that submerged leaves are thin and do not have clear differentiation of palisade tissue and spongy tissue. n Cross sections of submerged leaf vascular bundle and its magnification (o). White arrowheads indicate xylem and black arrowheads indicate phloem. P6 leaf was used for morphological and anatomical observations when plants were grown under a constant condition for 1.5–2 months. Bars 50 µm in a–f and bars 0.1 mm in h–o
Leaf morphological and anatomical characters of H. difformis.a Scanning electron micrographs of the abaxial side of a terrestrial leaf. Black circle indicates glandular trichome, white circle indicates nonglandular trichome. b Stomas and epidermal cells of the adaxial side of a terrestrial leaf. c Stomas and epidermal cells of the abaxial side of a terrestrial leaf. d Scanning electron micrographs of the abaxial side of a submerged leaf. Black circle shows glandular trichome. Note that only glandular trichomes grow on the submerged leaf lamina and midvein, and these trichomes are shorter than those on the terrestrial leaf. e Stomas and epidermal cells of the adaxial side of a submerged leaf. Note that epidermal cells of submerged leaves are smaller and have more lobes resulting in a more pronounced jigsaw shape. f Stomas and epidermal cells of the abaxial side of a submerged leaf. g Comparison of stomatal density: the number of stoma on both sides per unit area. Measured areas were 0.15 mm². Data are mean ± SD (n = 10). Bars marked with letters a, b or c are statistically different according to the Student’s t test (P < 0.05). h Cross sections of terrestrial leaf and its semithin section (i). Note that terrestrial leaves are thick and have obvious differentiation of palisade tissue and spongy tissue (j), cross sections of terrestrial leaf vascular bundle and its magnification (k). l Cross sections of submerged leaf and its semithin section (m). Note that submerged leaves are thin and do not have clear differentiation of palisade tissue and spongy tissue. n Cross sections of submerged leaf vascular bundle and its magnification (o). White arrowheads indicate xylem and black arrowheads indicate phloem. P6 leaf was used for morphological and anatomical observations when plants were grown under a constant condition for 1.5–2 months. Bars 50 µm in a–f and bars 0.1 mm in h–o
… 
Morphological and anatomical study of shoot and root of H. difformis. a Terrestrial stem with numerous trichomes on stem surface. White arrowheads indicate epidermal hairs. b Cross section of terrestrial stem. Black circle indicates aerenchyma, and black arrowhead indicates cortex layers. Note that the aerenchyma of terrestrial stems is surrounded by isometric cells and the cortex layers are thick. c Image of a terrestrial root. d Cross sections of terrestrial primary root. Note that no aerenchyma appears in the primary root. e Submerged stem observation showing absence of trichomes. f Cross sections of submerged stem. Black circle indicates aerenchyma. and black arrowhead indicates cortex layers. Note that the aerenchyma of submerged stems is surrounded by anisometric cells and the cortex layers are thin. g Image of a submerged root. h Cross sections of submerged primary root. Black circle indicates aerenchyma. Note that the aerenchyma of submerged primary root is lysigenous aerenchyma. Plants were grown under a constant condition for 1.5–2 months. Bars 1 mm
Morphological and anatomical study of shoot and root of H. difformis. a Terrestrial stem with numerous trichomes on stem surface. White arrowheads indicate epidermal hairs. b Cross section of terrestrial stem. Black circle indicates aerenchyma, and black arrowhead indicates cortex layers. Note that the aerenchyma of terrestrial stems is surrounded by isometric cells and the cortex layers are thick. c Image of a terrestrial root. d Cross sections of terrestrial primary root. Note that no aerenchyma appears in the primary root. e Submerged stem observation showing absence of trichomes. f Cross sections of submerged stem. Black circle indicates aerenchyma. and black arrowhead indicates cortex layers. Note that the aerenchyma of submerged stems is surrounded by anisometric cells and the cortex layers are thin. g Image of a submerged root. h Cross sections of submerged primary root. Black circle indicates aerenchyma. Note that the aerenchyma of submerged primary root is lysigenous aerenchyma. Plants were grown under a constant condition for 1.5–2 months. Bars 1 mm
… 
Comparison of leaf morphology at different temperatures. a Top view of submerged shoots. Left 26 °C, right 20 °C. b Comparison of submerged leaf morphology at 26 °C (upper) and 20 °C (lower). All silhouettes of leaves are based on photographic images. The oldest is at the left, and the youngest leaf is at the right. c Top view of terrestrial shoots. Left 26 °C, right 20 °C. d Comparison of terrestrial leaf morphologies at 26 °C (upper) and 20 °C (lower). All silhouettes of leaves are based on photographic images. The oldest is at the left, and the youngest leaf is at the right. Plants were grown under a constant condition for 1.5 months. Bars 1 cm
Comparison of leaf morphology at different temperatures. a Top view of submerged shoots. Left 26 °C, right 20 °C. b Comparison of submerged leaf morphology at 26 °C (upper) and 20 °C (lower). All silhouettes of leaves are based on photographic images. The oldest is at the left, and the youngest leaf is at the right. c Top view of terrestrial shoots. Left 26 °C, right 20 °C. d Comparison of terrestrial leaf morphologies at 26 °C (upper) and 20 °C (lower). All silhouettes of leaves are based on photographic images. The oldest is at the left, and the youngest leaf is at the right. Plants were grown under a constant condition for 1.5 months. Bars 1 cm
… 
Environmental factors affect leaf morphology. a Top view of terrestrial shoots. Left humidity shifted from 30 to 60% RH, right humidity shifted from 60 to 30% RH. b Leaves from a terrestrial plant shifted from 30 to 60% RH. Successive leaves are in phyllotactic order. Note that the leaf form is acquired acropetally within successive leaves. c Leaves from a terrestrial plant shifted from 60 to 30% RH. Successive leaves are in phyllotactic order. Note that successive leaves are increasingly less dissected. d Leaves from a submerged plant shifted from 20 to 26 °C. Note that the leaf form is acquired acropetally within successive leaves. e Leaves from a submerged plant shifted from 26 to 20 °C. Note that the leaf form is acquired acropetally within successive leaves. f Dissection index (DI) of successive leaves (P9 to P6) from plants switched to different conditions. Data are mean ± SD (n = 5). Note that DI is increasing when submerged plants are shifted from 26 to 20 °C and terrestrial plants shifted from 30 to 60% RH, while DI is decreasing when submerged plants are shifted from 20 to 26 °C and terrestrial plant shifted from 60 to 30% RH. White arrows indicate a leaf that displays intermediate morphology in response to environment shifts. Bars 1 cm
+2
Environmental factors affect leaf morphology. a Top view of terrestrial shoots. Left humidity shifted from 30 to 60% RH, right humidity shifted from 60 to 30% RH. b Leaves from a terrestrial plant shifted from 30 to 60% RH. Successive leaves are in phyllotactic order. Note that the leaf form is acquired acropetally within successive leaves. c Leaves from a terrestrial plant shifted from 60 to 30% RH. Successive leaves are in phyllotactic order. Note that successive leaves are increasingly less dissected. d Leaves from a submerged plant shifted from 20 to 26 °C. Note that the leaf form is acquired acropetally within successive leaves. e Leaves from a submerged plant shifted from 26 to 20 °C. Note that the leaf form is acquired acropetally within successive leaves. f Dissection index (DI) of successive leaves (P9 to P6) from plants switched to different conditions. Data are mean ± SD (n = 5). Note that DI is increasing when submerged plants are shifted from 26 to 20 °C and terrestrial plants shifted from 30 to 60% RH, while DI is decreasing when submerged plants are shifted from 20 to 26 °C and terrestrial plant shifted from 60 to 30% RH. White arrows indicate a leaf that displays intermediate morphology in response to environment shifts. Bars 1 cm
… 
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ORIGINAL ARTICLE
Water-Wisteria as an ideal plant to study heterophylly in higher
aquatic plants
Gaojie Li
1
•Shiqi Hu
1
•Jingjing Yang
1
•Elizabeth A. Schultz
2
•Kurtis Clarke
2
•
Hongwei Hou
1
Received: 11 January 2017 / Accepted: 22 April 2017 / Published online: 2 May 2017
ÓSpringer-Verlag Berlin Heidelberg 2017
Abstract
Key message The semi-aquatic plant Water-Wisteria is
suggested as a new model to study heterophylly due to
its many advantages and typical leaf phenotypic plas-
ticity in response to environmental factors and
phytohormones.
Abstract Water-Wisteria, Hygrophila difformis (Acan-
thaceae), is a fast growing semi-aquatic plant that exhibits
a variety of leaf shapes, from simple leaves to highly
branched compound leaves, depending on the environment.
The phenomenon by which leaves change their morphol-
ogy in response to environmental conditions is called
heterophylly. In order to investigate the characteristics of
heterophylly, we assessed the morphology and anatomy of
Hygrophila difformis in different conditions. Subsequently,
we verified that phytohormones and environmental factors
can induce heterophylly and found that Hygrophila dif-
formis is easily propagated vegetatively through either leaf
cuttings or callus induction, and the callus can be easily
transformed by Agrobacterium tumefaciens. These results
suggested that Hygrophila difformis is a good model plant
to study heterophylly in higher aquatic plants.
Keywords Hygrophila difformis Aquatic plant
Heterophylly Leaf Model plant Phytohormone
Introduction
Plants show considerable leaf form alteration in response to
changes in the surrounding environment, a phenotypic plas-
ticity called heterophylly (Zotz et al. 2011). Despite the gen-
eral trend to liveon dry land, some angiospermsreturned to the
water many years ago (Wissler et al. 2011). Plants that thrive
near the water, and are sometimes submerged by flooding, can
grow under water and in terrestrial conditions. Such plants
often display heterophylly, with submerged leaves having
quite different morphology and anatomy from leaves in ter-
restrial conditions. Heterophylly is generally regarded as an
important morphological process allowing adaptation to a
capricious environment (Nakayama et al. 2012).
There are many environmental changes associated with
terrestrial or submerged conditions, such as light quality
and intensity, availability of water and gases, and temper-
ature (Jo et al. 2010; Wanke 2011). Previous investigations
revealed that blue light and high intensity light induced the
development of terrestrial leaves in submersed Marsilea
quadrifolia and Hippuris vulgaris (Bodkin et al. 1980; Lin
and Yang 1999). Other reports suggested that a period of
darkness or continuous far-red light could cause Marsilea
vestita to develop the terrestrial form in a medium that
normally allows development of the aquatic form (Gaudet
1963). In addition, heterophylly is mediated by the effect of
daylength in Proserpinaca palustris (Schmidt and
Communicated by Xian Sheng Zhang.
Electronic supplementary material The online version of this
article (doi:10.1007/s00299-017-2148-6) contains supplementary
material, which is available to authorized users.
&Hongwei Hou
houhw@ihb.ac.cn
1
The State Key Laboratory of Freshwater Ecology and
Biotechnology, The Key Laboratory of Aquatic Biodiversity
and Conservation of Chinese Academy of Sciences, Institute
of Hydrobiology, Chinese Academy of Sciences, University
of Chinese Academy of Sciences, Wuhan 430072, Hubei,
People’s Republic of China
2
Department of Biological Sciences, University of Lethbridge,
Lethbridge, AB T1K 3M4, Canada
123
Plant Cell Rep (2017) 36:1225–1236
DOI 10.1007/s00299-017-2148-6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Heteromorphic leaves are an important and interesting manifestation of leaf morphology, which refers to the fact that plants with the same genotype grow different shaped leaves (e.g., lanceolate, ovate, and broad-ovate) along vertical heights (Hao et al., 2017;Iqbal et al., 2017). In nature, heteromorphic leaves are commonly found in aquatic plants in the transition zones between land and water (Li et al., 2017). It is believed that heteromorphic leaves reflect the plants' adaptation to environmental changes via their phenotypic plasticity (Zhao et al., 2021). ...
... It is believed that heteromorphic leaves reflect the plants' adaptation to environmental changes via their phenotypic plasticity (Zhao et al., 2021). The study of their change and formation mechanism can reveal the multiple effects of the environment on plants from gene to population (Li et al., 2017). Over the past multidecade, many studies have explored the functional and structural differences (i.e., anatomical structures, morphological and physiological traits) among different types of heteromorphic leaves and their responses to environmental changes (Niinemets et al., 2004;Liu et al., 2015;Xu et al., 2016). ...
... The morphology, physiology, and anatomical structure were quite different between the heteromorphic leaves. Such enormous phenotypic plasticity may make homogeneity less limiting to leaf trait variation (Li et al., 2017), resulting in the tradeoffs of paired leaf traits, such as stomatal size and density, that do not exhibit obvious coevolutionary relationships. ...
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... It is known that ABA signal pathways and transduction are conserved throughout the evolution of basal plants to angiosperms and function as important regulators for plant growth and stress response in many terrestrial species [26]. Furthermore, ABA was recently verified to be involved in the phenotypic plasticity of some aquatic plants, regulating their leaf shapes and stomata development and participating in their response to environmental changes [27][28][29]. Therefore, ABA seems to be an important regulator of the development and responses of aquatic plants to the surrounding environments. ...
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... In the amphibious plant Callitriche palustris [9], epidermal and mesophyll cells became longer along the proximal-distal axis under the submerged conditions. The submerged leaves of Hygrophila difformis have smaller epidermal pavement cells with more lobes, resulting in a more pronounced jigsaw shape [10]. In addition, leaf cross-sections showed a clear differentiation of palisade tissue only under terrestrial conditions; and a decrease of the mesophyll layer under the submerged conditions in this species. ...
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Heterophylly, the phenomenon by which plants alter leaf forms to adapt to surrounding conditions, is apparent in amphibious plant species. In response to submergence, they emerge leaves with narrower blade areas. The pathway that receives the submergence signals and the mechanism regulating leaf form via cell proliferation and/or expansion systems have not yet been fully identified yet. Our anatomical study of Rorippa aquatica, an amphibious plant that exhibits heterophylly in response to various signals, showed that leaf thickness increased upon submergence; this was caused by the expansion of mesophyll cell size. Additionally, these submergence effects were inhibited under blue-light conditions. The ANGUSTIFOLIA3 (AN3)/GROWTH-REGULATING FACTOR (GRF) pathway regulating cell proliferation and cell expansion was downregulated in response to submergence; and the response was blocked under the blue-light conditions. These results suggest that submergence and light quality determine leaf cell morphology via the AN3/GRF pathway.
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... Hypoxia leads to a reduction in leaf area due to limited absorption and transport of ions, resulting in mineral deficits for the shoots (Horchani et al. 2008). Additionally, the reduction in stomatal conductance, and the consequent decrease in the CO 2 assimilation rate, helps to explain the reduction in plant leaf area under flooded conditions (Li et al. 2017). ...
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Land plants have evolved the ability to cope with submergence. Amphibious plants are adapted to both aerial and aquatic environments through phenotypic plasticity in leaf form and function, known as heterophylly. In general, underwater leaves of amphibious plants are devoid of stomata, yet their molecular regulatory mechanisms remain elusive. Using the emerging model of the Brassicaceae amphibious species Rorippa aquatica, we lay the foundation for the molecular physiological basis of the submergence-triggered inhibition of stomatal development. A series of temperature shift experiments showed that submergence-induced inhibition of stomatal development is largely uncoupled from morphological heterophylly and likely regulated by independent pathways. Submergence-responsive transcriptome analysis revealed rapid reprogramming of gene expression, exemplified by the suppression of RaSPEECHLESS and RaMUTE within 1 h and the involvement of light and hormones in the developmental switch from terrestrial to submerged leaves. Further physiological studies place ethylene as a central regulator of the submergence-triggered inhibition of stomatal development. Surprisingly, red and blue light have opposing functions in this process: blue light promotes, whereas red light inhibits stomatal development, through influencing the ethylene pathway. Finally, jasmonic acid counteracts the inhibition of stomatal development, which can be attenuated by the red light. The actions and interactions of light and hormone pathways in regulating stomatal development in R. aquatica are different from those in the terrestrial species, Arabidopsis thaliana. Thus, our work suggests that extensive rewiring events of red light to ethylene signaling might underlie the evolutionary adaption to water environment in Brassicaceae.
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SHOOT MERISTEMLESS participates in the heterophylly of Hygrophila difformis (Acanthaceae)
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  • Aug 2022
In heterophyllous plants, leaf shape shows remarkable plasticity in response to environmental conditions. However, transgenic studies of heterophylly are lacking and the molecular mechanism remains unclear. Here, we cloned the KNOTTED1-LIKE HOMEOBOX family gene SHOOT MERISTEMLESS (STM) from the heterophyllous plant Hygrophila difformis (Acanthaceae). We used molecular, morphogenetic, and biochemical tools to explore its functions in heterophylly. HdSTM was detected in different organs of H. difformis, and its expression changed with environmental conditions. Heterologous, ectopic expression of HdSTM in Arabidopsis (Arabidopsis thaliana) increased leaf complexity and CUP-SHAPED COTYLEDON (CUC) transcript levels. However, overexpression of HdSTM in H. difformis did not induce the drastic leaf change in the terrestrial condition. Overexpression of HdSTM in H. difformis induced quick leaf variations in submergence, while knockdown of HdSTM led to disturbed leaf development and weakened heterophylly in H. difformis. HdCUC3 had the same spatiotemporal expression pattern as HdSTM. Biochemical analysis revealed a physical interaction between HdSTM and HdCUC3. Our results provide genetic evidence that HdSTM is involved in regulating heterophylly in H. difformis.
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A Decrease in Ambient Temperature Induces Post-Mitotic Enlargement of Palisade Cells in North American Lake Cress
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In order to maintain organs and structures at their appropriate sizes, multicellular organisms orchestrate cell proliferation and post-mitotic cell expansion during morphogenesis. Recent studies using Arabidopsis leaves have shown that compensation, which is defined as post-mitotic cell expansion induced by a decrease in the number of cells during lateral organ development, is one example of such orchestration. Some of the basic molecular mechanisms underlying compensation have been revealed by genetic and chimeric analyses. However, to date, compensation had been observed only in mutants, transgenics, and γ-ray-treated plants, and it was unclear whether it occurs in plants under natural conditions. Here, we illustrate that a shift in ambient temperature could induce compensation in Rorippa aquatica (Brassicaceae), a semi-aquatic plant found in North America. The results suggest that compensation is a universal phenomenon among angiosperms and that the mechanism underlying compensation is shared, in part, between Arabidopsis and R. aquatica.
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Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis
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Plant stem-cell pools, the source for all organs, are first established during embryogenesis. It has been known for decades that cytokinin and auxin interact to control organ regeneration in cultured tissue. Auxin has a critical role in root stem-cell specification in zygotic embryogenesis, but the early embryonic function of cytokinin is obscure. Here, we introduce a synthetic reporter to visualize universally cytokinin output in vivo. Notably, the first embryonic signal is detected in the hypophysis, the founder cell of the root stem-cell system. Its apical daughter cell, the precursor of the quiescent centre, maintains phosphorelay activity, whereas the basal daughter cell represses signalling output. Auxin activity levels, however, exhibit the inverse profile. Furthermore, we show that auxin antagonizes cytokinin output in the basal cell lineage by direct transcriptional activation of ARABIDOPSIS RESPONSE REGULATOR genes, ARR7 and ARR15, feedback repressors of cytokinin signalling. Loss of ARR7 and ARR15 function or ectopic cytokinin signalling in the basal cell during early embryogenesis results in a defective root stem-cell system. These results provide a molecular model of transient and antagonistic interaction between auxin and cytokinin critical for specifying the first root stem-cell niche.
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Regulation of the KNOX-GA Gene Module Induces Heterophyllic Alteration in North American Lake Cress
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Plants show leaf form alteration in response to changes in the surrounding environment, and this phenomenon is called heterophylly. Although heterophylly is seen across plant species, the regulatory mechanisms involved are largely unknown. Here, we investigated the mechanism underlying heterophylly in Rorippa aquatica (Brassicaceae), also known as North American lake cress. R. aquatica develops pinnately dissected leaves in submerged conditions, whereas it forms simple leaves with serrated margins in terrestrial conditions. We found that the expression levels of KNOTTED1-LIKE HOMEOBOX (KNOX1) orthologs changed in response to changes in the surrounding environment (e.g., change of ambient temperature; below or above water) and that the accumulation of gibberellin (GA), which is thought to be regulated by KNOX1 genes, also changed in the leaf primordia. We further demonstrated that exogenous GA affects the complexity of leaf form in this species. Moreover, RNA-seq revealed a relationship between light intensity and leaf form. These results suggest that regulation of GA level via KNOX1 genes is involved in regulating heterophylly in R. aquatica. The mechanism responsible for morphological diversification of leaf form among species may also govern the variation of leaf form within a species in response to environmental changes.
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Toward elucidating the mechanisms that regulate heterophylly
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  • Jan 2012
The leaves of some plant species are able to change their morphology in response to environmental conditions. This phenomenon is termed heterophylly. Various aquatic plants exhibit drastic changes in leaf shape in response to submerged aquatic conditions. Heterophyllic variation ranges from mere modification of leaf width to drastic alteration in the outline of leaves and is interpreted as an adaptation to aquatic habitats. Although this phenomenon is widely observed among angiosperms, there is limited information on the regulation of heterophyllic switch in leaf development. Here, we have reviewed existing knowledge on leaf development and heterophylly and have introduced Neobeckia aquatica as an emerging model to elucidate the mechanisms underlying heterophylly.
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LEAF DIMORPHISM IN THE AQUATIC ANGIOSPERM CALLITRICHE HETEROPHYLLA
Article
  • Sep 1985
Depending on the position of the shoot tip relative to the water surface, the aquatic angiosperm Callitriche heterophylla produces either ovate land-form or linear water-form leaves. This paper is concerned with the developmental basis for the leaf dimorphism of this species. Little significant difference is observed between the apical meristems of submerged vs. emergent shoots; moreover, land-form and water-form primordia undergo similar, if not identical, patterns of initial development until they attain a length of 350 to 400 μm. These findings are interpreted to mean that the divergent leaf forms result from the marked sensitivity of the primordia to their respective environments rather than from the mode of their inception. Subsequent growth of the young water-form leaf emphasizes longitudinal extension, while the immature land-form leaf continues balanced expansion in both longitudinal and lateral directions. The lateral growth of the land-form primordium is accomplished in part by a more persistent marginal meristem, but the morphological difference between the two leaf forms is mostly attributable to the difference in the predominant direction of intercalary expansion. In addition, certain anatomical features, such as vasculature, stomates, and cuticle, are much more prominent in mature land-form leaves than in water-form leaves. These anatomical differences seem to represent structural adaptations of each leaf form to the specific physiological requirements of its environment.
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Regulation of Leaf Shape in Proserpinaca palustris
Article
  • May 1968
Submerged shoots of Proserpinaca palustris have finely dissected leaves whether grown in long or short photoperiods, while leaves of aerial shoots are dissected in short days but expanded-lanceolate in long days. Shoot habit, internode length, and leaf orientation are also varied in these different environments. High light intensity or elevated temperature may induce aerial leaf shape and shoot morphology in long-day submerged shoots. When a shoot is transferred abruptly to a new environment a series of transitional leaf forms is produced. The number of transitional leaves depends on the number of immature leaves in the bud, which in turn depends on the environment in which the shoot had been growing. Leaf primordia in contrasting environments are identical in form until 500-600 μ. When the primordia are 500-600 μ long, five lobe pairs have been initiated in basipetal succession by accelerated cell division at sites along the marginal meristems. At this stage morphological differences become apparent; these involve differential distribution of cell division in lobes and sinus regions. Cell surface replicas revealed only limited differences in cell shape in dissected and expanded aerial leaves. However, in pinnatifid submerged leaves, polar elongation of cells of the lobes and midrib is associated with the larger, more finely dissected leaf form. Further, long-day leaves develop more lobes than short-day leaves, and the rate of leaf development per plastochron is faster in long-day shoots. Heterophylly of amphibious plants is discussed, including possible mechanisms by which the environmental stimulus may regulate the elemental processes of cell division and polar cell expansion which are involved in shaping the leaf.
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Leaf Dimorphism in the Aquatic Angiosperm Callitriche heterophylla
Article
  • Sep 1985
Depending on the position of the shoot tip relative to the water surface, the aquatic angiosperm Callitriche heterophylla produces either ovate land-form or linear water-form leaves. The developmental basis for this leaf dimorphism is examined. -from Authors
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