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THE HOT AND THE CLASSIC

There are few examples of developmental plasticity in plants as dramatic as the heterophylly exhibited by many aquatic plants. In general, round-shaped and thick leaves with stomata are observed in dry upland conditions, whereas thin elongate leaves that are often highly dissected and which bear few or no stomata, are formed under submerged conditions. Heterophylly is observed in a wide range of vascular plants ranging from the fern Marsilea quadrifolia to diverse angiosperm lineages, including both dicots and monocots. The widespread occurrence of heterophylly across distantly related taxa suggests that heterophylly, in many cases, has arisen from convergent evolution. Heterophylly may increase the fitness of aquatic plants by decreasing leaf damage from mechanical forces or herbivores, by decreasing water loss or by enhancing photosynthesis. Cook and Johnson (1968) provided evidence that those populations of aquatic plants that routinely experience the greatest heterogeneity in water levels also exhibit the greatest degree of heterophylly. The reduction of heterophylly in populations from more stable environments suggests that there may be energetic costs associated with heterophylly (DeWitt et al., 1998). Regardless of its functional role in the ecology of the species, heterophyllous leaf development provides a highly amenable system for studying developmental plasticity in plants.

Hormonal Induction of Heterophylly

Because heterophylly has apparently arisen many times by convergent evolution, it is not surprising that different factors contribute to the induction of heterophylly in different species. Given that the leaves of submerged plants experience relatively dry conditions upon emerging above the surface of the water, it might be expected that the drought hormone abscisic acid (ABA) would play a role in the induction of heterophylly. Indeed, the application of ABA to heterophyllous aquatic plants has been reported to initiate the production of terrestrial-type leaves in all the species examined to date (e.g. Anderson, 1978; Young and Horton, 1985; Kane and Albert, 1987; Kuwabara et al., 2003). Goliber and Feldman (1989) reported that ABA levels increased in the leaves of aerially stressed specimens of Hippuris vulgaris. Other hormones have also been implicated in regulating the induction of heterophylly. Gibberellic acid (GA) has been reported to affect leaf morphology in an opposite way to ABA in a few species (Allsop, 1962; Deschamp and Cooke, 1984). In Eichornia crassipes, however, GA promotes the formation of terrestrial-type leaves (Watson et al., 1982). Wells and Pigliucci (2000) have suggested that the effects of GA in this case may be a reflection of the short-day induction of the submerged leaf type that occurs in this species. More recently, Kuwabara et al. (2003) examined the effects of ethylene and ABA upon heterophyllous leaf formation of Ludwigia arcuata. Treatment with ethylene gas resulted in the formation of submerged-type leaves on terrestrial shoots of L. arcuata, whereas treatments with ABA induced the formation of terrestrial-type leaves on submerged shoots. Measurement of the endogenous ethylene concentration of submerged shoots showed that it was higher than that of terrestrial ones. In contrast, the endogenous ABA concentration of terrestrial shoots was higher than that of submerged ones.

Other Factors Inducing Heterophylly

Many other factors play a role in the induction of aerial leaf type morphology in heterophyllous aquatic species. Those environmental conditions that typify the summer, including high temperatures (e.g. Deschamp and Cooke, 1984; Goliber and Feldman, 1990; Kane and Albert, 1982), long photoperiods (Bostrock and Millington, 1962; Cook, 1969; Webb, 1984) and high light intensities (e.g. Goliber, 1989), generally induce the aerial-type leaf morphology in a range of species.

Light quality can also be influential in inducing heterophylly. Lin and Yang (1999) reported that blue light and ABA independently induce heterophylly in Marsilea quadrifolia. Fluridone, an inhibitor of ABA synthesis, did not prevent blue light induction of aerial-type leaves. Moreover, during blue light treatments, the ABA levels in the leaves remained unchanged. Phytochrome has also been implicated in the induction of heterophylly in some species (Gaudet, 1963; Bodkin et al., 1980; Goliber and Feldman, 1990). Because the attenuation of far-red light is greater in deep water, phytochrome responsiveness in terms of the induction of heterophylly may be of greater importance to aquatics growing in deeper waters (Wells and Pigliucci, 2000).

Other authors have reported a role for osmotic stress in inducing aerialleaf type morphology (e.g. McCully and Dale, 1961; Deschamp and Cooke, 1984.

Molecular Biology of Heterophylly

Studies of the molecular biological changes associated with the induction of heterophylly in the model organism Marsilea quadrifolia are just beginning (Hsu et al., 2001). Marsilea produces different types of leaves in response to changes in natural environment and culture conditions. When conditions are conducive, the exogenous application of ABA induces the formation of aerial-type leaves. The tissues responsive to ABA are localized in the shoot apical meristem and the associated organ primordia. Hsu et al. (2001) identified at least two tiers of ABA-regulated early genes from these tissues, including seven primary genes and seventeen secondary genes. These genes, designated ABRH for ABA-responsive heterophylly, showed diverse expression patterns during the course of heterophyllous induction. Changes in the transcript level of ABRH genes started within 0.5–1.0 h after the addition of ABA to the culture medium. Some changes were transient while the others were persistent. The ABRH genes contain extensive sequence homology to known genes, including those encoding transcription factors, protein kinases, membrane transporters, metabolic enzymes, structural proteins, and those encoded by the chloroplast genome. A number of other genes identified in this study have not been previously reported to relate to ABA responses: These include genes involved in transcriptional regulation, signal transduction, membrane transport, and metabolism.

Peter V. Minorsky

Department of Natural Sciences Mercy College Dobbs Ferry, NY 10522

FOOTNOTES

www.plantphysiol.org/cgi/doi/10.1104/pp.900096.

LITERATURE CITED

Allsop A (1962) The effects of gibberellic acid on morphogenesis in Marsilea drummondi A. Phytomorphology 12: 1-10

Anderson LWJ (1978) Abscisic acid induces formation of floating leaves in the heterophyllous aquatic angiosperm Potamageton nodosus. Science 201: 1135-1138[Abstract/Free Full Text]

Bodkin PC, Spence DHN, Weeks DC (1980) Photoreversible control of heterophylly in Hippuris vulgaris L. New Phytol 84: 533-542[CrossRef]

Bostrack JM, Millington WF (1962) On the determination of leaf form in the aquatic heterophyllous species of Ranunculus. Bull Torrey Bot Club 89: 1-20

Cook CDK (1969) On the determination of leaf form in Ranunculus aquatilis. New Phytol 68: 469-480

Cook SA, Johnson MP (1968) Adaptation to heterogenous environments I. Variation in heterophylly in Ranunculus flammula L. Evolution 22: 496-516[CrossRef][Web of Science]

Deschamp PA, Cooke TJ (1984) Causal mechanisms of leaf dimorphism in the aquatic Callitriche heterophylla. Am J Bot 71: 319-329[CrossRef]

DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13: 77-81

Gaudet JJ (1963) Marsilea vestita: Conversion of the water form to the land form by darkness and by far-red light. Science 140: 975-976[Abstract/Free Full Text]

Goliber TE (1989) Endogenous ABA content correlates with photon fluence rate and induced leaf morphology in Hippuris vulgaris. Plant Physiol 89: 732-734[Abstract/Free Full Text]

Goliber TE, Feldman LJ (1989) Osmotic stress, endogenous abscisic acid, and the control of leaf morphology in Hippuris vulgaris L. Plant Cell Environ 12: 163-171[CrossRef][Medline]

Goliber TE, Feldman LJ (1990) Developmental analysis of leaf plasticity in the heterophyllous aquatic plant Hippuris vulgaris L. Am J Bot 77: 399-412[CrossRef]

Hsu TC, Liu HC, Wang JS, Chen RW, Wang YC, Lin BL (2001) Early genes responsive to abscisic acid during heterophyllous induction in Marsilea quadrifolia. Plant Mol Biol 47: 703-715[CrossRef][Web of Science][Medline]

Kane ME, Albert LS (1982) Environmental and growth regulator effects on heterophylly and growth of Proserpinaca intermedia (Haloragaceae) Hippuris vulgaris L. Aquat Bot 23: 73-85[CrossRef]

Kane ME, Albert LS (1987) Abscisic acid induces aerial leaf morphology and vascularization in submerged Hippuris vulgaris L. Aquat Bot 28: 81-88

Kuwabara A, Ikegami K, Koshiba T, Nagata T (2003) Effects of ethylene and abscisic acid upon heterophylly in Ludwigia arcuata (Onagraceae). Planta 217: 880-887[CrossRef][Web of Science][Medline]

Lin BL, Yang WJ (1999) Blue light and abscisic acid independently induce heterophyllous switch in Marsilea quadrifolia. Plant Physiol 119: 429-434[Abstract/Free Full Text]

McCully ME, Dale HM (1961) Heterophylly in Hippuris, a problem in identification. Can J Bot 39: 1099-1116

Watson MA, Carrier JC, Cook GL (1982) Effect of exogenously supplied gibberellic acid (GA₃) on patterns of water hyacinth development. Aquat Bot 13: 57-68

Webb CJ (1984) Heterophylly in Eryngium vesiculosum (Umbelliferae). New Zeal J Bot 22: 29-33

Wells CL, Pigliucci M (2000) Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants. Persp Plant Ecol Evol Syst 3: 1-18

Young JP, Horton RF (1985) Heterophylly in Ranunculus flabellaris: the effect of abscisic acid. Ann Bot 55: 899-902[Abstract/Free Full Text]

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