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

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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
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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
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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.
... Substantial cellular changes in the aerial and submerged leaves were not observed following the application of hormones, although slight elongations and narrowing were detected that were consistent with the leaf forms ( Figure 3, F, H, and I; Supplemental Figures S5 and S6). Previous research on other aquatic plants proved that some submerged-like leaf phenotypes, such as a significantly narrow or compounded leaf form or extensive decreases in stomatal density, can be induced by a simple hormonal perturbation in many cases (Kuwabara et al., 2001;Sato et al., 2008;Nakayama et al., 2014;Li et al., 2017;Kim et al., 2018;Horiguchi et al., 2019). Therefore, our results suggest that the extent of the hormonal contribution to heterophylly differs between C. palustris and previously investigated amphibious plants. ...
... Recent studies clarified the molecular basis of heterophylly in several distant lineages of aquatic plants. In R. aquatica and Hygrophila difformis, the compound leaf forms of submerged plants are associated with the transcriptional activation of class I KNOX genes in leaves (Nakayama et al., 2014;Li et al., 2017). However, orthologs of these genes are not expressed in the simple leaves of C. palustris leaves under submerged conditions. ...
... For example, when needle leaf ludwigia (Ludwigia arcuata, Onagraceae) is treated with ethylene gas or ACC under aerial growth conditions, the plants produce submerged-type leaves, indicating that ethylene signaling almost sufficiently induces submerged-type leaf development in this species (Kuwabara et al., 2003;Sato et al., 2008). Similarly, treating the aerial parts of R. trichophyllus and water wisteria (Hygrophila defformis, Acanthaceae) plants with ethylene induces drastic changes in some leaf phenotypes, which are similar to those observed in submerged leaves to some extent (Li et al., 2017;Kim et al., 2018;Horiguchi et al., 2019). The involvement of ethylene is reasonable because, under submerged conditions, ethylene spontaneously accumulates in the plant body because of the limited gas exchange in water (Jackson, 1985). ...
Article
Full-text available
Heterophylly is the development of different leaf forms in a single plant depending on the environmental conditions. It is often observed in amphibious aquatic plants that can grow under both aerial and submerged conditions. Although heterophylly is well recognized in aquatic plants, the associated developmental mechanisms and the molecular basis remain unclear. To clarify these underlying developmental and molecular mechanisms, we analyzed heterophyllous leaf formation in an aquatic plant, Callitriche palustris. Morphological analyses revealed extensive cell elongation and the rearrangement of cortical microtubules in the elongated submerged leaves of C. palustris. Our observations also suggested that gibberellin, ethylene, and abscisic acid all regulate the formation of submerged leaves. However, the perturbation of one or more of the hormones was insufficient to induce the formation of submerged leaves under aerial conditions. Finally, we analyzed gene expression changes during aerial and submerged leaf development and narrowed down the candidate genes controlling heterophylly via transcriptomic comparisons, including a comparison with a closely related terrestrial species. We discovered that the molecular mechanism regulating heterophylly in C. palustris is associated with hormonal changes and diverse transcription factor gene expression profiles, suggesting differences from the corresponding mechanisms in previously investigated amphibious plants.
... 9-020-02527 -x) contains supplementary material, which is available to authorized users. examples of heterophylly are found in aquatic and amphibious plants, in which submerged leaves are always dissected, thin, narrow and lack stomata, whereas terrestrial leaves are simple, thicker, expanded and have abundant stomata (Wells and Pigliucci 2000;Wanke 2011;Li et al. 2017Li et al. , 2019a. Heterophylly is an extreme example of the leaf shape changes that occur in all plants in order to optimize physiological function to the environment, so heterophylly provides an ideal process to understand the mechanism by which plants acclimate their growth to withstand environmental changes (Kuwabara et al. 2003;Wanke 2011;Kim et al. 2018). ...
... Heterophylly is observed in a large number of aquatic plants, including those in Brassicales, Euphorbiales, Marsileales, Myrtiflorae, Nymphaeales, Ranales and Tubiflorae (Cook 1969;Deschamp and Cooke 1984;Lin and Yang 1999;Kuwabara et al. 2001;Titus et al. 2001;Nakayama et al. 2014;Li et al. 2017). Many environmental factors, like humidity, temperature, CO 2 and light are involved in regulating heterophylly. ...
... Many environmental factors, like humidity, temperature, CO 2 and light are involved in regulating heterophylly. For example, high humidity can significantly change the leaf shape of Hygrophila difformis from serrated to highly dissected forms (Li et al. 2017). Low temperature or high CO 2 can induce deep-lobed aquatic leaves of Ranunculus flabellaris in terrestrial conditions (Johnson 1967;Bristow 1969). ...
Article
Full-text available
Key message: This is the first report of a highly efficient Agrobacterium tumefaciens-mediated transformation protocol for Acanthaceae and its utilization in revealing important roles of cytokinin in regulating heterophylly in Hygrophila difformis. Plants show amazing morphological differences in leaf form in response to changes in the surrounding environment, which is a phenomenon called heterophylly. Previous studies have shown that the aquatic plant Hygrophila difformis (Acanthaceae) is an ideal model for heterophylly study. However, low efficiency and poor reproducibility of genetic transformation restricted H. difformis as a model plant. In this study, we reported successful induction of callus, shoots and the establishment of an efficient stable transformation protocol as mediated by Agrobacterium tumefaciens LBA4404. We found that the highest callus induction efficiency was achieved with 1 mg/L 1-Naphthaleneacetic acid (NAA) and 2 mg/L 6-benzyladenine (6-BA), that efficient shoot induction required 0.1 mg/L NAA and 0.1 mg/L 6-BA and that high transformation efficiency required 100 µM acetosyringone. Due to the importance of phytohormones in the regulation of heterophylly and the inadequate knowledge about the function of cytokinin (CK) in this process, we analyzed the function of CK in the regulation of heterophylly by exogenous CK application and endogenous CK detection. By using our newly developed transformation system to detect CK signals, contents and distribution in H. difformis, we revealed an important role of CK in environmental mediated heterophylly.
... Heterophylly is found in many plants, especially aquatic plants, and its molecular mechanism has recently been reported (e.g. Li et al., 2017;Koga et al., 2021). Rorippa aquatica (Brassicaceae) is a perennial herbaceous and semiaquatic plant whose habitat includes the shores of lakes, ponds, and streams in North America that exhibits distinct heterophylly between submerged and terrestrial conditions (Nakayama et al., 2014). ...
... Therefore, it is quite possible that the heterophylly induced by KNOX1 will be the target of selection and that its fixation will lead to morphological diversification. As mentioned above, molecular mechanisms that regulate heterophylly have now been reported (Nakayama et al., 2014;Li et al., 2017;Koga et al., 2021), and our knowledge of epigenetic mechanisms independent of sequence variation is accumulating as well. These studies demonstrate the utility of examining developmental systems within their ecological context, which will better inform our understanding of the evolutionary events leading to morphological diversification. ...
Article
Full-text available
Abstrvact The basic mechanisms of leaf development have been revealed through a combination of genetics and intense analyses in select model species. The genetic basis for diversity in leaf morphology seen in nature is also being unraveled through recent advances in techniques and technologies related to genomics and transcriptomics, which have had a major impact on these comparative studies. However, this has led to the emergence of new unresolved questions about the mechanisms that generate the diversity of leaf form. Here, we provide a review of the current knowledge of the fundamental molecular genetic mechanisms underlying leaf development with an emphasis on natural variation and conserved gene regulatory networks involved in leaf development. Beyond that, we discuss open questions/enigmas in the area of leaf development, how recent technologies can best be deployed to generate a unified understanding of leaf diversity and its evolution, and what untapped fields lie ahead.
... How aquatic plants form such different leaves has been investigated among various eudicots, such as Ranunculus species (Ranunculaceae; Young and Horton, 1985;Young et al., 1987;Kim et al., 2018), Rorippa aquatica (Brassicaceae; Nakayama et al., 2014), Hygrophila difformis (Acanthaceae; Li et al., 2017;Horiguchi et al., 2019), Ludwigia arcuata (Onagraceae; Kuwabara et al., 2001Kuwabara et al., , 2003Kuwabara and Nagata, 2006;Sato et al., 2008), Rumex palustris (Polygonaceae; Peeters et al., 2002;Voesenek et al., 2003;Cox et al., 2004Cox et al., , 2006Vreeburg et al., 2005), Hippuris vulgaris (Plantaginaceae; McCully and Dale, 1961;Kane and Albert, 1987;Goliber, 1989;Goliber and Feldman, 1990), and Callitriche species (Plantaginaceae; Jones, 1952Jones, , 1955aDeschamp and Cooke, 1983, 1984. In addition, many monocots (e.g., Alismatales and Poales) and even basal angiosperms (i.e., Nymphaeales) are known to show an extensive heterophylly (Arber, 1920;Sculthorpe, 1967), and have been subjected to morphological and physiological studies (Inamdar and Aleykutty, 1979;Titus and Sullivan, 2001;Iida et al., 2009Iida et al., , 2016He et al., 2018). ...
... Although the major hormones gibberellin, abscisic acid (ABA), and ethylene are generally involved in the heterophylly among these plants, the roles of these hormones may vary (Wanke, 2011;Nakayama et al., 2017). For example, R. aquatica and H. difformis show the opposite gibberellin responses (Nakayama et al., 2014;Li et al., 2017). Thus, it is worthwhile to assess adaptations to aquatic environments across various plant lineages. ...
Article
Full-text available
Heterophylly, or phenotypic plasticity in leaf form, is a remarkable feature of amphibious plants. When the shoots of these plants grow underwater, they often develop surprisingly different leaves from those that emerge in air. Among aquatic plants, it is typical for two or more distinct leaf development processes to be observed in the same individual exposed to different environments. Here, we analyze the developmental processes of heterophylly in the amphibious plant Callitriche palustris L. (Plantaginaceae). First, we reliably cultured this species under laboratory conditions and established a laboratory strain. We also established a framework for molecular-based developmental analyses, such as whole-mount in situ hybridization. We observed several developmental features of aerial and submerged leaves, including changes in form, stomata and vein formation, and transition of the meristematic zone. Then we defined developmental stages for C. palustris leaves. We found that in early stages, aerial and submerged leaf primordia had similar forms, but became discriminable through cell divisions with differential direction, and later became highly distinct via extensive cell elongation in submerged leaf primordia.
... 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). ...
Article
Full-text available
Key message The species did not show a response pattern to flooding. Andira anthelmia and Vernonanthura discolor invested in plastic responses, while Guarea guidonia established a balance between integration and phenotypic plasticity. Abstract Dense ombrophilous forests are tropical phytophysiognomies that make up the vegetation mosaic of the Brazilian Atlantic Forest. These forests occur in humid regions and often contain flooded areas that impose obstacles to plant colonization. Some species such as Guarea guidonia (Meliaceae), Andira anthelmia (Fabaceae), and Vernonanthura discolor (Asteraceae) can tolerate these flooding conditions. However, little is known about the acclimatization of these species to flooding. For this reason, morphoanatomical and physiological analyses were performed on the leaves of five individuals of each species selected from a flooded and non-flooded site. The results showed that the species presented thicker leaves and higher specific leaf mass values under flooding conditions. However, it was observed that the thickening of G. guidonia and V. discolor is mainly influenced by the palisade parenchyma thickness, while in A. anthelmia thickening was more closely related to the spongy parenchyma thickness. Greater thickening of the cuticle and epidermis and greater density of stomata were also observed in the flooded site. The chlorophyll a and b and carotenoid contents were significantly lower in the flooded site. Chloroplasts exhibited higher amounts of starch grain, lipid drops, and plastoglobules in the flooded site. Regarding the quantum yield of photosystems II, only A. anthelmia showed a reduction in Fv/Fm values in the flooded site. Plasticity and phenotypic integration analyses made it possible to conclude that the acclimatization of A. anthelmia and V. discolor was mainly mediated by plastic adjustments. At the same time, G. guidonia presented greater phenotypic integration.
... CKs were discovered to act downstream of the KNOTTEDLIKE HOMEOBOX (KNOX1) transcription factors in delaying the leaf maturation process [72,73]. KNOX1 genes are responsible for stem cell maintenance in the SAM and leaf development by regulating CKs and gibberellin (GA) [74,75]. It was reported that the KNOX1-CK/GA module also plays important role in the regulation of heterophylly (a typical representative of leaf plasticity) in many aquatic plants, such as Hygrophila difformis [76][77][78] and Rorippa aquatica [79,80]. ...
Article
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Auxins and cytokinins (CKs) are the most influential phytohormones, having multifaceted roles in plants. They are key regulators of plant growth and developmental processes. Additionally, their interplay exerts tight control on plant development and differentiation. Although several reviews have been published detailing the auxin-cytokinin interplay in controlling root growth and differentiation, their roles in the shoot, particularly in leaf morphogenesis are largely unexplored. Recent reports have provided new insights on the roles of these two hormones and their interplay on leaf growth and development. In this review, we focus on the effect of auxins, CKs, and their interactions in regulating leaf morphogenesis. Additionally, the regulatory effects of the auxins and CKs interplay on the phyllotaxy of plants are discussed.
... 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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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.
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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