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CAM photosynthesis in submerged aquatic plants

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Abstract

Crassulacean acid metabolism (CAM) is a CO2-concentrating mechanism selected in response to aridity in terrestrial habitats, and, in aquatic environments, to ambient limitations of carbon. Evidence is reviewed for its presence in five genera of aquatic vascular plants, includingIsoëtes, Sagittaria, Vallisneria, Crassula, andLittorella. Initially, aquatic CAM was considered by some to be an oxymoron, but some aquatic species have been studied in sufficient detail to say definitively that they possess CAM photosynthesis. CO2-concentrating mechanisms in photosynthetic organs require a barrier to leakage; e.g., terrestrial C4 plants have suberized bundle sheath cells and terrestrial CAM plants high stomatal resistance. In aquatic CAM plants the primary barrier to CO2 leakage is the extremely high difrusional resistance of water. This, coupled with the sink provided by extensive intercellular gas space, generates daytime CO2(pi) comparable to terrestrial CAM plants. CAM contributes to the carbon budget by both net carbon gain and carbon recycling, and the magnitude of each is environmentally influenced. Aquatic CAM plants inhabit sites where photosynthesis is potentially limited by carbon. Many occupy moderately fertile shallow temporary pools that experience extreme diel fluctuations in carbon availability. CAM plants are able to take advantage of elevated nighttime CO2 levels in these habitats. This gives them a competitive advantage over non-CAM species that are carbon starved during the day and an advantage over species that expend energy in membrane transport of bicarbonate. Some aquatic CAM plants are distributed in highly infertile lakes, where extreme carbon limitation and light are important selective factors.

Compilation of reports on diel changes in titratable acidity and malate show 69 out of 180 species have significant overnight accumulation, although evidence is presented discounting CAM in some. It is concluded that similar proportions of the aquatic and terrestrial floras have evolved CAM photosynthesis. AquaticIsoëtes (Lycophyta) represent the oldest lineage of CAM plants and cladistic analysis supports an origin for CAM in seasonal wetlands, from which it has radiated into oligotrophic lakes and into terrestrial habitats. Temperate Zone terrestrial species share many characteristics with amphibious ancestors, which in their temporary terrestrial stage, produce functional stomata and switch from CAM to C3. Many lacustrineIsoëtes have retained the phenotypic plasticity of amphibious species and can adapt to an aerial environment by development of stomata and switching to C3. However, in some neotropical alpine species, adaptations to the lacustrine environment are genetically fixed and these constitutive species fail to produce stomata or loose CAM when artificially maintained in an aerial environment. It is hypothesized that neotropical lacustrine species may be more ancient in origin and have given rise to terrestrial species, which have retained most of the characteristics of their aquatic ancestry, including astomatous leaves, CAM and sediment-based carbon nutrition.

Resumen

El metabolismo ácido Crasulacea (cam) es un mecanismo concentrador de CO2 seleccionado en respuesta a la aridez de hábitats terrestres, y, en ambientes acuáticos, a limitaciones de carbono en el medio. Se revisa la evidencia para su presencia en cinco géneros de plantas vasculares acuáticas, incluyendoIsoëtes, Sagitteria, Vallisneria, Crassula yLittorella. Inicialmente, el CAM acuático era considerado absurdo, pero algunas especies han sido estudiadas a detalle suficiente para determinar definitivamente que poseen fotosíntesis CAM. Los mecanismos concentradores de CO2 en órganos fotosintéticos requieren de barreras contra la fuga del mismo; por ejemplo, plantas terrestres C4 tienen células con una capa de cera y las plantas terrestres CAM poseen una alta resistencia en los estomas. En las plantas acuáticas la principal barrera para la fuga de CO2 es la resistencia a la difusión extremadamente alta del agua. Esto, junto con el resumidero proporcionado por el amplio espacio gaseoso intercelular, genera CO2(pi) diurno comparable a plantas terrestres CAM. CAM contribuye al presupuesto de carbono tanto por la ganancia neta de carbono como por su reciclaje, la magnitud de cada componente está influida por el ambiente. Las plantas cam acuáticas habitan en sitios donde la fotosíntesis está potencialmente limitada por carbono. Muchas ocupan piscinas temporales poco profundas y moderadamente fértiles, que experimentan fluctuaciones diálicas extremas en la disponibilidad de carbono. Las plantas CAM son capaces de aprovechar los altos niveles nocturnos de CO2 en estos hábitats, potencialmente adquiriendo una ventaja competitiva sobre las plantas no poseedoras de CAM, las cuales sufren la falta de carbono durante el día, o sobre las especies que utilizan energía en el transporte de bicarbonato a través de membranas. Otras plantas CAM acuáticas se encuentran distribuidas en lagos altamente infértiles, en los que la limitation extrema de carbono y luz son factores de selección importantes.

La compilation de reportes sobre cambios diólicos en ácido titulable y malato muestran que 69 de 180 especies tienen una acumulación nocturna signifícativa, aunque la evidencia es presentada descontando CAM en algunos casos. Se concluye que proporciones similares de las floras terrestres y acuáticas han evolucionado fotosíntesis CAM.Isoëtes acuática (Lycophyta) representa el linaje más antiguo de plantas CAM, y el análisis cladístico apoya la idea del origen de CAM en humedales estacionales, de donde radiaron a lagos oligotróficos y a hábitats terrestres. Las especies terrestres de zonas templadas comparten muchas características con sus ancestros anfibios, las cuales en su estado terrestre temporal producen estomas funcionales y cambian de CAM a C3. MuchasIsoëtes lacustres han retenido la plasticidad fenotipica de especies anfibias y pueden adaptarse a una ambiente aéreo al desarrollar estomas y cambiar a C3. Sin embrago, en algunas especies neotropicales alpinas, las adaptaciones al ambiente lacustre están determinadas géniticamente y estas especies fallan en producir estomas o perder CAM al mantenerlas artificialmente en un ambiente aéreo. Se presenta la hipótesis que éstas son de origen anterior y han dado lugar a las especies terrestres que retienen la mayorma de las características de su estado ancestral acuático, incluyendo hojas sin estomas, CAM y nutrición de carbono basado en sedimentos.

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  1. Jon E. Keeley (Research Scientist/Station Leader)

    Present address: USGS Biological Resources Division, Sequoia-Kings Canyon Field Station, 93271, Three Rivers, CA, USA

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Keeley, J.E. CAM photosynthesis in submerged aquatic plants. Bot. Rev 64, 121–175 (1998). https://doi.org/10.1007/BF02856581

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