Heterophylly: Phenotypic Plasticity of Leaf Shape in Aquatic and Amphibious Plants
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plants Review Heterophylly: Phenotypic Plasticity of Leaf Shape in Aquatic and Amphibious Plants 1, 1, 1 2,3, Gaojie Li y, Shiqi Hu y, Hongwei Hou and Seisuke Kimura * 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, China; [email protected] (G.L.); [email protected] (S.H.); [email protected] (H.H.) 2 Faculty of Life Sciences, Kyoto Sangyo University, Kamigamo-motoyama, Kita-ku, Kyoto-shi, Kyoto 603-8555, Japan 3 Center for Ecological Evolutionary Developmental Biology, Kyoto Sangyo University, Kamigamo-motoyama, Kita-ku, Kyoto-shi, Kyoto 603-8555, Japan * Correspondence: [email protected]; Tel.: +81-75-705-3113 These authors contributed equally to this work. y Received: 21 August 2019; Accepted: 14 October 2019; Published: 16 October 2019 Abstract: Leaves show great diversity in shape, size, and color in nature. Interestingly, many plant species have the ability to alter their leaf shape in response to their surrounding environment. This phenomenon is termed heterophylly, and is thought to be an adaptive feature to environmental heterogeneity in many cases. Heterophylly is widespread among land plants, and is especially dominant in aquatic and amphibious plants. Revealing the mechanisms underlying heterophylly would provide valuable insight into the interaction between environmental conditions and plant development. Here, we review the history and recent progress of research on heterophylly in aquatic and amphibious plants. Keywords: heterophylly; submergence; environment; adaptation; molecular mechanisms 1. What is Heterophylly? Plants display amazing morphological diversity of leaves. The leaves of some plant species can undergo considerable form alteration in response to environmental conditions via a process called heterophylly (Figure1)[ 1]. Heterophylly is a type of phenotypic plasticity that is widespread among plants. Heterophyllous plants produce dramatic, often abrupt changes in leaf morphology in response to environmental factors [1]. Interestingly, most known examples of heterophylly are found in aquatic and amphibious plants, in which submerged leaves are often dissected compared with simple terrestrial leaves [2] (Table 1). Because these plants are sometimes submerged during flooding, they have evolved to thrive and grow both under water and terrestrial conditions. Such plants often display heterophylly, which is generally regarded as a morphological process allowing adaptation to a capricious environment [2,3]. Leaf shapes are related to their function, as submerged leaves are thin, narrow, and lack cuticles and stomata, whereas terrestrial leaves are thicker, expanded, and cutinized with stomata [2,3]. An example is the narrow leaves of amphibious plants located along riverbanks where flooding always occurs. Narrow leaves are less efficient at absorbing sunlight than those that have wider blades; however, they can withstand the destructive force of water flow. Narrow or deeply serrated/lobed leaves are also present in aquatic plants, and may provide for similar interactions with the surrounding environment, including factors beyond the submerged conditions for mineral Plants 2019, 8, 420; doi:10.3390/plants8100420 www.mdpi.com/journal/plants Plants 2019, 8, x FOR PEER REVIEW 2 of 14 Plants 2019, 8, 420 2 of 13 for mineral nutrient and CO2 uptake. These narrow or dissected leaf blade formations are likely an adaptation to underwater conditions. nutrient and CO2 uptake. These narrow or dissected leaf blade formations are likely an adaptation to underwater conditions. Figure 1. Heterophylly of amphibious plant, North American lake cress, Rorippa aquatica (Brassicaceae). North American lake cress shows distinct heterophylly between submerged and terrestrialFigure 1. conditions.Heterophylly Leaf of shape amphibious alternation plant, is also North induced American by changes lake incress, ambient Rorippa temperature. aquatica Bars,(Brassicaceae 1cm. ). North American lake cress shows distinct heterophylly between submerged and terrestrial conditions. Leaf shape alternation is also induced by changes in ambient temperature. Bars, The1cm. original definition of heterophylly was not strictly linked to the environment, and lacked a clear distinction from other similar processes [1]. However, heterophylly was recently defined as leaf form alterationThe original in responsedefinition to of environmental heterophylly was conditions, not strictly unlike linked heteroblasty to the environment, and anisophylly and lacked [1,4–6]. a Heteroblastyclear distinction was from described other as similar changes processes in leaf shape [1]. However, during growth heterophylly development, was recently but does defined not include as leaf morphologicalform alteration changes in response induced to environmental by environmental conditions, factors unlike [1,5 ].heteroblasty Similarly, and anisophylly anisophylly is usually [1,4–6]. coupledHeteroblasty with asymmetry was described and phyllotaxis as changes of in leaves leaf andshape stems, during and growth also does development, not include morphological but does not changesinclude inducedmorphological by environmental changes induced factors [by7]. environmental factors [1,5]. Similarly, anisophylly is usuallyConsidering coupled thewith distinct asymmetry differences and phyllotaxis in leaf shape of leaves between and aerial stems, and and submerged also does conditions,not include elucidatingmorphological the mechanisms changes induced underlying by environmental heterophylly factors in aquatic [7]. and amphibious plants would provide valuableConsidering insight into the the distinct interaction differences between in the leaf environment shape between and plantaerial development.and submerged conditions, elucidating the mechanisms underlying heterophylly in aquatic and amphibious plants would 2.provide History valuable of Research insight on into Heterophylly the interaction between the environment and plant development. Heterophylly is observed in many evolutionary diverse aquatic and amphibious plant species including2. History those of Research belonging on Heterophylly to the Nymphaeales, Ranunculales, Saxifragales, Myrtales, Brassicales, Lamiales,Heterophylly and many is other observed orders in [ 8many–16] (Table evolutionary1). There diverse are remarkable aquatic and morphological amphibious di plantfferences species in theseincluding heterophyllous those belonging plants between to the Nymphaeales, submerged and Ranunculales, terrestrial environments. Saxifragales, Leaves Myrtales, under submergedBrassicales, conditionsLamiales, tendand many to have other a thin, orders filamentous, [8–16] (Table or linear 1). T shape,here are degraded remarkable vascular morphological structure, and differences the leaves in usuallythese heterophyllous lack stomata cells, plant whichs between means plantssubmerged must directly and terrestrial absorb nutrients environments. and exchange Leaves gas under from watersubmerged [2,3,17 ,conditions18]. Here, wetend review to have the a existingthin, filamentous knowledge, or of linear heterophylly shape, degraded in different vascular species, structure with a , particularand the leaves focus onusually the role lack of phytohormonesstomata cells, which and environmental means plants factorsmust directly in regulating absorb heterophylly, nutrients and to gainexchang valuablee gas insight from water into this [2,3,1 phenomenon.7,18]. Here, we review the existing knowledge of heterophylly in different species, with a particular focus on the role of phytohormones and environmental factors in regulating heterophylly, to gain valuable insight into this phenomenon. Plants 2019, 8, 420 3 of 13 Table 1. Representative heterophyllous plants and treatments that can induce heterophylly. Species Family Common Name Treatments References Alisma graminifolium Alismataceae - light [19] two-headed ABA, GA, temperature, osmotic Callitriche heterophylla Callitrichaceae [11,20,21] water-starwort stress narrowleaf Callitriche intermedia Callitrichaceae osmotic stress, temperature [22,23] water-starwort Callitriche stagnalis Callitrichaceae pond water starwort GA [20,21] ABA, temperature, light intensity, Hippuris vulgaris Hippuridaceae common mare’s tail [5,9,24,25] R/FR ratio, osmotic stress ABA, ethylene, GA, humidity, Hygrophila difformis Acanthaceae Water-Wisteria [26,27] temperature Ilex aquifolium Aquifoliaceae Common holly mammalian browsing [28] piedmont Ludwigia arcuata Onagraceae ABA, ethylene, temperature [6,14,29,30] primrose-willow Marsilea quadrifolia Marsileaceae European water clover ABA, blue light, CO2 [12,13] Marsilea vestita Marsileaceae hairy water clover CO2, light intnsity, light quality [31,32] red stemmed parrot Myriophyllum brasiliense Haloragaceae CO [33] feather 2 CO , sediment type and water Nuphar variegate Nymphaeaceae yellow water lily 2 [34] depth Nuphar lutea Nymphaeaceae yellow pond-lily water depth [16] Potamogeton nodosus Potamogetonaceae longleaf pondweed ABA [4] Potamogeton alpinus Potamogetonaceae - water flow [35] submerged or floating condition, Potamogeton octandrus Potamogetonaceae - [36] development ABA, GA, light intensity, Proserpinaca palustris Haloragidaceae marsh mermaid-weed humidity, osmotic stress, [17,37,38] photoperiod intermediate Proserpinaca intermedia Haloragidaceae photoperiod